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library(GOstats) # GO term hypergeometric tests - load early so it doesn't clash with dplyr::select etc
library(WGCNA) # Gene networks - needs 'impute' dependency: source("https://bioconductor.org/biocLite.R"); biocLite("impute")
library(RSQLite) # Access SQLite databases
library(reshape2) # data tidying (melt)
library(dplyr) # data tidying
library(tidyr) # data tidying
library(stringr) # string manipulation
library(ggplot2) # for plots
library(ggrepel) # for plots
library(ggdendro) # for plots
library(gridExtra) # for plots
library(RColorBrewer) # for plots
library(ggjoy) # for plots
library(gplots) # Venn diagram
library(ecodist) # for nmds
library(MuMIn) # for model comparison
library(sva) # for ComBat function; install via source("https://bioconductor.org/biocLite.R"); biocLite("sva")
library(pander) # for nice tables
library(kableExtra) # For scrollable tables
kable.table <- function(df) {
kable(df, "html") %>%
kable_styling() %>%
scroll_box(height = "300px")
}
# Open database connections (Sasha uses SQL, Luke prefers dplyr)
db <- dbConnect(SQLite(), dbname="data/queen_pheromone.db")
my_db <- src_sqlite("data/queen_pheromone.db")
# These 4 samples should NOT be used (See below). They were also removed in all non-R analyses (e.g. differential gene expression analyses using EBseq)
bad.samples <- c("lf1", "ln1", "ln12", "lf12")
# Define a function to get gene expression data for a given set of orthologous genes. We define orthologous genes as those that are each other's reciprocal best BLAST. The bad.samples argument can be used to remove some named samples. By default this function logs the expression data (using log10). It returns a list with two elements: the first element is a matrix of expression data (rows = samples, cols = genes), and the second is a data frame giving the species-specific names of the orthologous genes
make.OGGs <- function(species, bad.samples = NULL, log.data = T){
# set up forward mappings, e.g. "am2bt", "am2lf", "am2ln"
forward.mappings <- paste(species[1], "2", species[2:length(species)], sep = "")
# and reverse mappings, e.g. "bt2am", "lf2am", "ln2am"
backward.mappings <- paste(species[2:length(species)], "2", species[1], sep = "")
items <- list() # declare empty list
for(i in 1:length(forward.mappings)){
# make a table with 3 columns: first column has species 1 gene,
# second column has species 2 gene in forward mapping,
# third column has species 2 gene in reverse mapping (this can be NA, or different to col 2)
# we want the rows where cols 2 and 3 are the same, indicating reciprocity in the BLAST
focal <- left_join(
tbl(my_db, forward.mappings[i]) %>%
dplyr::select(-evalue), # get the two mappings and
tbl(my_db, backward.mappings[i]) %>%
dplyr::select(-evalue), # merge by species 1 column
by = species[1]
) %>%
collect(n=Inf) %>% as.data.frame # collect it all and convert to df
# Get the RBB rows, and keep the two relevant columns
focal <- focal[!is.na(focal[,3]), ]
items[[i]] <- focal[focal[,2] == focal[,3], 1:2]
}
rbbs <- items[[1]] # If 3 or 4 species, successively merge the results
if(length(items) > 1) rbbs <- left_join(rbbs, items[[2]], by = species[1])
if(length(items) > 2) rbbs <- left_join(rbbs, items[[3]], by = species[1])
# Throw out species1 genes that do not have a RBB in all species
rbbs <- rbbs[complete.cases(rbbs), ]
names(rbbs) <- gsub("[.]x", "", names(rbbs)) # tidy the row and column names
rownames(rbbs) <- NULL
# Make sure the columns are ordered as in 'species'
rbbs <- rbbs[, match(names(rbbs), species)]
# We know have a list of the names of all the ortholgous genes in each species
# Now we use these names to look up the gene expression data for each ortholog
expression.tables <- paste("rsem_", species, sep = "")
for(i in 1:length(species)){
focal.expression <- tbl(my_db, expression.tables[i]) %>%
collect(n=Inf) %>% as.data.frame()
names(focal.expression)[names(focal.expression) == "gene"] <- species[i]
rbbs <- left_join(rbbs, focal.expression, by = species[i])
}
gene.name.mappings <- rbbs[, names(rbbs) %in% species] # save gene name mappings in separate DF
rownames(rbbs) <- rbbs[,1] # Use the gene names for species 1 as row names
rbbs <- rbbs[, !(names(rbbs) %in% species)] # remove gene name columns
rbbs <- t(as.matrix(rbbs))
if(log.data) rbbs <- log10(1 + rbbs)
if(!is.null(bad.samples)) rbbs <- rbbs[!(rownames(rbbs) %in% bad.samples), ]
# Discard genes where NAs appear
gene.name.mappings <- gene.name.mappings[!(is.na(colSums(rbbs))), ]
rbbs <- rbbs[, !(is.na(colSums(rbbs)))]
# discard genes where expression is zero for all samples in 1 or more species
spp <- str_replace_all(rownames(rbbs), "[:digit:]", "")
to.keep <- rep(TRUE, ncol(rbbs))
for(i in 1:ncol(rbbs)){
if(min(as.numeric(tapply(rbbs[,i], spp, sum))) == 0) to.keep[i] <- FALSE
}
rbbs <- rbbs[, to.keep]
gene.name.mappings <- gene.name.mappings[to.keep, ]
list(tpm = rbbs, gene.mappings = gene.name.mappings)
}
Closer inspection reveals that they have zeros for many of the transcripts, so perhaps they had low abundance libraries.
set.seed(1) # nmds involves random numbers, so make this plot reproducible
expression.data <- make.OGGs(c("am", "bt", "ln", "lf"))[[1]]
treatments <- tbl(my_db, "treatments") %>% as.data.frame()
shhh <- capture.output(nmds.output <- dist(expression.data) %>% nmds())
data.frame(id = rownames(expression.data), nmds.output$conf[[length(nmds.output$conf)]], stringsAsFactors = F) %>%
left_join(treatments, by = "id") %>%
rename(Species = species, Treatment = treatment) %>%
ggplot(aes(X1,X2, shape = Species)) +
geom_point(aes(colour = Treatment)) +
geom_text_repel(aes(label = id), size=3.6) +
xlab("NMDS 1") + ylab("NMDS 2")
Figure S1: After reducing the transcriptome data to two axes using non-metric multidimensional scaling, four Lasius samples are clear outliers.
set.seed(1) # nmds involves random numbers, so make this plot reproducible
expression.data <- make.OGGs(c("am", "bt", "ln", "lf"), bad.samples = bad.samples)[[1]]
shhh <- capture.output(nmds.output <- dist(expression.data) %>% nmds())
data.frame(id = rownames(expression.data),
nmds.output$conf[[length(nmds.output$conf)]],
stringsAsFactors = F) %>%
left_join(treatments, by = "id") %>%
rename(Species = species, Treatment = treatment) %>%
ggplot(aes(X1,X2)) +
geom_point(aes(shape = Species, colour = Treatment)) +
geom_text_repel(aes(label = id), size=3.6) +
xlab("NMDS 1") + ylab("NMDS 2")
Figure S2: With the four problematic samples removed, the samples cluster according to species with no obvious outliers.
Table S1: Number of sequencing libraries for each combination of species and treatment, after removing the four problematic libraries. Each library was prepared from a pool of workers, taken from the same colony.
sample.size.table <- treatments[treatments$id %in% rownames(expression.data),] %>%
group_by(species, treatment) %>%
summarise(n = n()) %>% as.data.frame()
names(sample.size.table) <- c("Species", "Treatment", "Number of RNAseq libraries")
sample.size.table %>% pander()
| Species | Treatment | Number of RNAseq libraries |
|---|---|---|
| am | Control | 3 |
| am | QP | 3 |
| bt | Control | 5 |
| bt | QP | 5 |
| lf | Control | 7 |
| lf | QP | 6 |
| ln | Control | 5 |
| ln | QP | 5 |
apis.de <- suppressMessages(tbl(my_db, "ebseq_padj_gene_am") %>%
select(gene, PostFC) %>%
left_join(tbl(my_db, "bee_names")) %>%
collect() %>%
mutate(PostFC = round(log2(PostFC), 3)) %>%
select(gene, name, PostFC) %>%
rename(Gene=gene, Name=name, Log2_FC = PostFC) %>%
arrange(-abs(Log2_FC))) %>% as.data.frame()
bombus.de <- suppressMessages(tbl(my_db, "ebseq_padj_gene_bt") %>%
select(gene, PostFC) %>%
left_join(tbl(my_db, "bt2am") %>% rename(gene=bt)) %>%
left_join(tbl(my_db, "bee_names") %>% rename(am=gene)) %>%
collect() %>%
mutate(PostFC = round(log2(PostFC), 3), name = replace(name, is.na(name), " "),
am = replace(am, is.na(am), " ")) %>%
select(gene, am, name, PostFC) %>%
rename(Gene=gene, Apis_BLAST=am, Name=name, Log2_FC = PostFC) %>%
arrange(-abs(Log2_FC))) %>% as.data.frame()
flavus.de <- suppressMessages(tbl(my_db, "ebseq_padj_gene_lf") %>%
select(gene, PostFC) %>%
left_join(tbl(my_db, "lf2am") %>% rename(gene=lf)) %>%
left_join(tbl(my_db, "bee_names") %>% rename(am=gene)) %>%
collect() %>%
mutate(PostFC = round(log2(PostFC), 3), name = replace(name, is.na(name), " "),
am = replace(am, is.na(am), " ")) %>%
select(gene, am, name, PostFC) %>%
rename(Gene=gene, Apis_BLAST=am, Name=name, Log2_FC = PostFC) %>%
arrange(-abs(Log2_FC))) %>% as.data.frame()
niger.de <- suppressMessages(tbl(my_db, "ebseq_padj_gene_ln") %>%
select(gene, PostFC) %>%
left_join(tbl(my_db, "ln2am") %>% rename(gene=ln)) %>%
left_join(tbl(my_db, "bee_names") %>% rename(am=gene)) %>%
collect() %>%
mutate(PostFC = round(log2(PostFC), 3), name = replace(name, is.na(name), " "),
am = replace(am, is.na(am), " ")) %>%
select(gene, am, name, PostFC) %>%
rename(Gene=gene, Apis_BLAST=am, Name=name, Log2_FC = PostFC) %>%
arrange(-abs(Log2_FC))) %>% as.data.frame()
names(apis.de) <- gsub("_", " ", names(apis.de))
names(bombus.de) <- gsub("_", " ", names(bombus.de))
names(flavus.de) <- gsub("_", " ", names(flavus.de))
names(niger.de) <- gsub("_", " ", names(niger.de))
Table S2: List of the 322 significantly differentially expressed genes (EBseq; p < 10-5) in Apis mellifera, listed in order of fold change in gene expression on a Log\(_2\) scale. Positive fold change values indicate higher expression in the control, while negative values indicate higher expression in the queen pheromone treatment.
kable.table(apis.de)
| Gene | Name | Log2 FC |
|---|---|---|
| GB55204 | Major royal jelly protein 3 | 6.480 |
| GB51373 | bypass of stop codon protein 1-like | 5.385 |
| GB50604 | uncharacterized protein LOC724113 | 3.775 |
| 102655911 | uncharacterized protein LOC102655911 | -3.376 |
| GB49819 | branched-chain-amino-acid aminotransferase, cytosolic-like | 2.657 |
| 102656917 | uncharacterized LOC102656917, transcript variant X1 | 2.609 |
| GB54417 | dehydrogenase/reductase SDR family member 11-like isoform X1 | 2.242 |
| GB45565 | chymotrypsin-2 | 2.052 |
| GB53886 | protein G12-like isoform X4 | 1.983 |
| 100576536 | uncharacterized protein LOC100576536 | 1.945 |
| GB41540 | venom carboxylesterase-6-like | -1.721 |
| GB54690 | uncharacterized protein LOC408547 | -1.583 |
| GB54150 | uncharacterized protein LOC408462 | -1.560 |
| GB43639 | uncharacterized protein LOC100577506 isoform X1 | -1.557 |
| GB49548 | serine/threonine-protein phosphatase 2B catalytic subunit 3-like isoform X11 | -1.455 |
| GB49878 | probable cytochrome P450 6a14 isoformX1 | 1.393 |
| GB53414 | serine/threonine-protein kinase ICK-like isoform X2 | 1.357 |
| 102654781 | protein G12-like | 1.324 |
| 102656058 | uncharacterized protein PF11_0213-like | -1.311 |
| GB53957 | U6 snRNA-associated Sm-like protein LSm1-like | 1.276 |
| GB50413 | protein TBRG4-like isoform X1 | -1.261 |
| 102653931 | uncharacterized LOC102653931, transcript variant X2 | -1.258 |
| GB53876 | interaptin-like | -1.209 |
| GB42705 | protein archease-like | 1.184 |
| 101664701 | PI-PLC X domain-containing protein 1-like isoform X1 | 1.143 |
| GB42523 | uncharacterized LOC100577781, transcript variant X2 | -1.130 |
| 102654405 | protein G12-like | 1.115 |
| 100578075 | uncharacterized LOC100578075 | -1.110 |
| GB52251 | multifunctional protein ADE2, transcript variant X2 | 1.088 |
| GB40764 | uncharacterized protein LOC414021 isoform X7 | -1.086 |
| GB55648 | Down syndrome cell adhesion molecule-like protein Dscam2-like isoform X7 | -1.084 |
| 726446 | uncharacterized protein LOC726446 | -1.063 |
| GB54467 | probable G-protein coupled receptor 52 isoform 1 | -1.060 |
| GB46985 | 60S ribosomal protein L12 isoform X1 | 1.045 |
| GB55191 | uncharacterized protein LOC100576289 | -1.045 |
| GB54890 | kynurenine 3-monooxygenase isoform X2 | 1.016 |
| GB55640 | retinol dehydrogenase 12-like | -1.006 |
| 724802 | protein Asterix-like | 0.996 |
| GB40010 | titin-like isoform X2 | -0.967 |
| 102654949 | uncharacterized protein LOC102654949 | 0.967 |
| GB43234 | histone deacetylase 5 isoform X8 | -0.965 |
| GB52266 | furin-like protease 2-like | -0.927 |
| GB41706 | ice-structuring glycoprotein-like | -0.926 |
| GB42673 | retinol dehydrogenase 10-A-like isoform X4 | 0.923 |
| GB55030 | uncharacterized protein LOC725074 | 0.921 |
| 551123 | RNA-binding protein Musashi homolog Rbp6-like isoform X1 | -0.920 |
| 409728 | 40S ribosomal protein S5 isoform X1 | 0.917 |
| GB45028 | venom dipeptidyl peptidase 4 | -0.898 |
| GB53422 | ufm1-specific protease 1-like isoform X2 | 0.892 |
| GB48933 | methenyltetrahydrofolate synthase domain-containing protein-like | -0.876 |
| GB53077 | cysteine-rich protein 1-like | 0.871 |
| GB41301 | annexin-B9-like | 0.862 |
| GB51748 | dentin sialophosphoprotein | -0.861 |
| 102654594 | WD repeat-containing protein 18-like | 0.852 |
| GB50356 | 60S acidic ribosomal protein P2 | 0.837 |
| GB44091 | LOW QUALITY PROTEIN: uncharacterized protein LOC408779 | -0.836 |
| GB41151 | protein MNN4-like | -0.834 |
| 409202 | ribosomal protein S9, transcript variant X2 | 0.834 |
| GB44340 | small ubiquitin-related modifier 3 isoform 1 | 0.833 |
| GB49173 | 4-aminobutyrate aminotransferase, mitochondrial-like isoform X2 | -0.826 |
| GB40769 | dehydrogenase/reductase SDR family member 11-like | 0.823 |
| GB54243 | LOW QUALITY PROTEIN: carbonyl reductase [NADPH] 1-like | 0.819 |
| 724531 | 40S ribosomal protein S28-like | 0.812 |
| GB51744 | uncharacterized protein LOC724439 | 0.811 |
| GB51947 | uncharacterized protein LOC724835 isoform X2 | -0.807 |
| GB40875 | 60S ribosomal protein L10 isoform X1 | 0.806 |
| 102655694 | glutathione S-transferase-like | 0.803 |
| GB55827 | 40S ribosomal protein S21-like isoform X1 | 0.801 |
| 102654426 | 60S ribosomal protein L18-like | 0.801 |
| GB49988 | SRR1-like protein-like isoform X2 | -0.800 |
| GB55963 | uncharacterized protein LOC725224 isoform X1 | -0.797 |
| GB50867 | cell differentiation protein RCD1 homolog isoform X2 | 0.794 |
| GB43256 | ATP-binding cassette sub-family D member 1-like | 0.792 |
| GB41211 | ATP-binding cassette sub-family E member 1 | 0.787 |
| GB52314 | gamma-tubulin complex component 4 | -0.785 |
| 102654251 | uncharacterized protein LOC102654251 | -0.782 |
| 726860 | cytochrome b5-like isoform 1 | 0.778 |
| GB46039 | tubulin alpha-1 chain-like | 0.773 |
| GB53358 | protein transport protein Sec61 subunit gamma-like isoform X3 | 0.768 |
| GB48699 | 60S ribosomal protein L11-like | 0.767 |
| GB44311 | actin related protein 1 | 0.762 |
| 102655603 | transmembrane emp24 domain-containing protein 7-like | 0.762 |
| GB49170 | 40S ribosomal protein S15Aa-like isoform 1 | 0.758 |
| GB47736 | alkyldihydroxyacetonephosphate synthase-like | 0.753 |
| GB49013 | RNA-binding protein 8A | 0.752 |
| 724485 | probable small nuclear ribonucleoprotein E-like | 0.749 |
| GB53000 | ubiquitin-60S ribosomal protein L40 isoform 2 | 0.749 |
| 725936 | titin-like | -0.748 |
| GB50158 | 60S ribosomal protein L4 isoform 1 | 0.748 |
| GB52432 | KN motif and ankyrin repeat domain-containing protein 3-like isoform X3 | -0.746 |
| 724757 | histone H4-like | 0.745 |
| GB53219 | 40S ribosomal protein S17 | 0.742 |
| 100577623 | putative uncharacterized protein DDB_G0282133-like isoform X2 | -0.742 |
| GB51038 | 60S ribosomal protein L23 | 0.739 |
| GB40284 | cytochrome P450 6a2 | 0.737 |
| GB50709 | 40S ribosomal protein S19a | 0.735 |
| GB50977 | probable tubulin polyglutamylase TTLL2-like | -0.734 |
| GB42537 | 40S ribosomal protein S15 | 0.734 |
| GB42467 | phospholipase B1, membrane-associated-like isoform X2 | 0.733 |
| GB41886 | protein transport protein Sec61 subunit alpha isoform 2 | 0.729 |
| GB51201 | 40S ribosomal protein S12 isoform X1 | 0.724 |
| GB55183 | ankyrin repeat domain-containing protein SOWAHB-like isoform X5 | -0.724 |
| GB54814 | 60S ribosomal protein L31 isoform 1 | 0.721 |
| GB49159 | probable nuclear transport factor 2-like isoform 3 | 0.717 |
| GB52512 | 60S ribosomal protein L28 | 0.714 |
| GB41142 | probable dolichyl pyrophosphate Glc1Man9GlcNAc2 alpha-1,3-glucosyltransferase-like isoform X2 | 0.712 |
| GB51359 | 60S ribosomal protein L27a isoform X1 | 0.710 |
| GB50519 | transmembrane emp24 domain-containing protein eca-like | 0.710 |
| GB47638 | ER membrane protein complex subunit 3-like | 0.705 |
| GB51046 | probable signal peptidase complex subunit 2-like | 0.701 |
| GB54973 | selT-like protein-like isoform 1 | 0.693 |
| GB44661 | intracellular protein transport protein USO1 isoform X9 | -0.691 |
| GB53953 | mitochondrial coenzyme A transporter SLC25A42-like isoformX1 | -0.688 |
| GB48289 | uncharacterized protein LOC726292 isoform X1 | 0.688 |
| GB47808 | DEP domain-containing protein 5 isoform X4 | -0.685 |
| GB45937 | intracellular protein transport protein USO1 isoform X2 | -0.684 |
| GB53750 | UPF0454 protein C12orf49 homolog isoform X2 | 0.682 |
| GB50455 | ubiquitin-conjugating enzyme E2-17 kDa-like | 0.676 |
| GB42356 | arginine-glutamic acid dipeptide repeats protein-like | -0.675 |
| GB51072 | 40S ribosomal protein S4-like isoform 1 | 0.669 |
| GB55268 | 43 kDa receptor-associated protein of the synapse homolog isoform X3 | -0.669 |
| GB43086 | uncharacterized protein LOC726486 | 0.668 |
| 102655259 | 5-methylcytosine rRNA methyltransferase NSUN4-like isoform X1 | -0.667 |
| GB55639 | 40S ribosomal protein S3 | 0.666 |
| GB41159 | bifunctional dihydrofolate reductase-thymidylate synthase | 0.665 |
| GB42354 | ATP-dependent Clp protease ATP-binding subunit clpX-like, mitochondrial-like isoform X4 | -0.663 |
| GB42696 | 60S ribosomal protein L35a isoform X3 | 0.656 |
| GB42088 | 40S ribosomal protein S29-like isoform X2 | 0.652 |
| GB53948 | uncharacterized protein LOC410057 isoform X1 | -0.651 |
| GB47553 | electron transfer flavoprotein subunit alpha, mitochondrial-like isoform 1 | 0.650 |
| 100577163 | slit homolog 2 protein-like | 0.650 |
| GB52627 | protein pigeon-like | -0.650 |
| GB54020 | apolipoprotein D-like | 0.650 |
| 102655440 | uncharacterized protein LOC102655440 | -0.649 |
| GB51009 | T-complex protein 1 subunit delta-like isoform 1 | 0.649 |
| GB49583 | 40S ribosomal protein S14 | 0.647 |
| GB41039 | 60S ribosomal protein L17 isoform 1 | 0.647 |
| GB46627 | paraplegin-like | -0.645 |
| GB54174 | E3 ubiquitin-protein ligase RING1 isoform 1 | 0.643 |
| GB41240 | aquaporin AQPAn.G-like isoform X3 | -0.641 |
| GB51440 | proteoglycan 4-like | -0.641 |
| GB45433 | small ribonucleoprotein particle protein B | 0.638 |
| GB51603 | peptidyl-alpha-hydroxyglycine alpha-amidating lyase 1-like isoform X5 | -0.638 |
| 100191002 | ribosomal protein L41 | 0.638 |
| GB43989 | serine-threonine kinase receptor-associated protein-like | 0.637 |
| GB53799 | proteasome subunit alpha type-2 | 0.636 |
| GB43141 | uncharacterized protein LOC413428 | -0.636 |
| GB44999 | chascon-like | -0.633 |
| GB49154 | bcl-2-related ovarian killer protein homolog A | 0.632 |
| GB50189 | epsilon-sarcoglycan | -0.630 |
| GB41150 | 40S ribosomal protein S2 isoform 2 | 0.628 |
| GB50917 | 60S acidic ribosomal protein P1 | 0.627 |
| GB48201 | 39S ribosomal protein L53, mitochondrial | 0.627 |
| GB44575 | ankyrin repeat and zinc finger domain-containing protein 1-like isoform X1 | -0.626 |
| GB46776 | 40S ribosomal protein S11 isoform X1 | 0.624 |
| GB49789 | 28S ribosomal protein S29, mitochondrial isoformX1 | -0.621 |
| GB46750 | 40S ribosomal protein S16 | 0.620 |
| GB44749 | 60S ribosomal protein L9 | 0.618 |
| GB44931 | evolutionarily conserved signaling intermediate in Toll pathway, mitochondrial-like | -0.613 |
| GB46845 | 60S ribosomal protein L37a | 0.611 |
| GB43379 | membrane-bound transcription factor site-2 protease-like | 0.609 |
| GB45369 | receptor of activated protein kinase C 1, transcript variant X3 | 0.606 |
| GB52698 | synaptobrevin-like isoformX1 | 0.605 |
| 724829 | immediate early response 3-interacting protein 1-like isoform X1 | 0.605 |
| GB49536 | gamma-secretase subunit Aph-1 | 0.604 |
| GB55628 | probable RNA-binding protein EIF1AD-like isoform X1 | 0.603 |
| GB50832 | THO complex subunit 4-like | 0.602 |
| GB50929 | mitochondrial import receptor subunit TOM40 homolog 1-like isoform 1 | 0.601 |
| GB51065 | 40S ribosomal protein S10-like isoform 1 | 0.601 |
| GB54984 | chromatin complexes subunit BAP18-like isoform X1 | 0.600 |
| GB43180 | minor histocompatibility antigen H13-like | 0.597 |
| GB49365 | gamma-secretase subunit pen-2 isoform 1 | 0.595 |
| GB51543 | 60S ribosomal protein L13a isoform 2 | 0.594 |
| GB54341 | RNA-binding protein 33-like | -0.594 |
| 102655912 | L-aminoadipate-semialdehyde dehydrogenase-phosphopantetheinyl transferase-like | 0.593 |
| GB53420 | uncharacterized protein LOC100576355 isoformX2 | -0.591 |
| GB48370 | ATP-binding cassette sub-family B member 7, mitochondrial isoform X1 | -0.591 |
| 726369 | peptidyl-tRNA hydrolase 2, mitochondrial-like isoform 1 | -0.591 |
| GB46478 | tectonin beta-propeller repeat-containing protein isoform X1 | -0.591 |
| GB42736 | TM2 domain-containing protein CG10795-like | 0.588 |
| GB49087 | formin-binding protein 1 homolog isoform X7 | -0.588 |
| GB50753 | uncharacterized LOC408705 | -0.586 |
| GB46123 | endonuclease G, mitochondrial-like | -0.586 |
| GB48574 | thioredoxin-2 isoform 1 | 0.586 |
| GB43232 | transmembrane protein 222-like isoform 1 | 0.586 |
| GB45285 | eukaryotic translation initiation factor 3 subunit F-like | 0.584 |
| GB44631 | uroporphyrinogen-III synthase-like | 0.582 |
| GB49994 | 60S ribosomal protein L26 | 0.581 |
| GB52563 | ATP-dependent helicase brm | -0.579 |
| GB54723 | uncharacterized protein LOC726790 isoform X1 | -0.578 |
| GB53668 | translocator protein-like | 0.577 |
| GB45374 | 40S ribosomal protein S23-like | 0.576 |
| GB46984 | ribonuclease UK114-like isoform 1 | 0.572 |
| 102655352 | uncharacterized protein LOC102655352 | -0.572 |
| GB45037 | beta-lactamase-like protein 2-like isoform X2 | -0.572 |
| GB52107 | tubulin alpha-1 chain-like | 0.571 |
| GB54139 | flocculation protein FLO11-like | -0.565 |
| 410017 | protein OPI10 homolog | 0.564 |
| GB49177 | 60S ribosomal protein L27 isoform X2 | 0.557 |
| GB54221 | transmembrane protein 50A-like | 0.556 |
| GB54979 | 60S ribosomal protein L21 | 0.555 |
| GB48111 | proteasome subunit beta type-1 | 0.552 |
| GB48745 | 5’-nucleotidase domain-containing protein 3-like | -0.550 |
| GB47079 | hexokinase type 2-like isoform X3 | -0.549 |
| GB47441 | V-type proton ATPase 21 kDa proteolipid subunit-like | 0.549 |
| GB41207 | 26S proteasome non-ATPase regulatory subunit 14 | 0.549 |
| GB50274 | transitional endoplasmic reticulum ATPase TER94 | 0.544 |
| GB51683 | annexin-B9-like isoform X1 | 0.544 |
| GB54952 | proteasome subunit alpha type-1-like | 0.543 |
| GB52253 | protein PRRC2C-like isoform X2 | -0.542 |
| GB41648 | protein chibby homolog 1-like | 0.542 |
| GB41363 | 26S protease regulatory subunit 6B isoform 1 | 0.541 |
| GB53247 | transmembrane emp24 domain-containing protein-like | 0.541 |
| GB48983 | RING finger protein 121-like isoform X3 | 0.541 |
| GB50873 | 60S ribosomal protein L30 isoform 1 | 0.540 |
| GB54255 | uncharacterized protein LOC551488 | 0.540 |
| GB48810 | 60S ribosomal protein L8 | 0.537 |
| GB41894 | uncharacterized protein LOC411277 isoform X28 | -0.536 |
| GB49021 | cuticular protein precursor | 0.536 |
| GB50131 | phosphatidate phosphatase PPAPDC1A-like isoform X2 | 0.535 |
| GB41811 | filaggrin-like isoform X3 | -0.534 |
| GB51484 | protein mago nashi | 0.528 |
| GB46705 | muscle M-line assembly protein unc-89 isoform X5 | -0.526 |
| GB45978 | dynein light chain Tctex-type isoform X2 | 0.526 |
| GB43449 | signal recognition particle 9 kDa protein | 0.526 |
| GB48150 | actin-related protein 2/3 complex subunit 1A | 0.525 |
| GB54854 | proteasome maturation protein-like | 0.523 |
| GB51545 | dystrophin, isoforms A/C/F/G/H-like | -0.523 |
| GB49095 | high affinity copper uptake protein 1-like isoformX1 | 0.523 |
| GB43638 | protein enhancer of sevenless 2B | 0.522 |
| GB51994 | proteasome subunit beta type-6-like | 0.520 |
| GB53194 | 60S ribosomal protein L14 isoform X2 | 0.519 |
| 102656618 | uncharacterized protein LOC102656618 isoform X1 | -0.518 |
| GB40539 | 40S ribosomal protein S20 | 0.518 |
| GB41631 | 60S ribosomal protein L34 isoform X2 | 0.518 |
| GB43938 | cytosolic endo-beta-N-acetylglucosaminidase-like isoform X4 | 0.516 |
| GB45878 | tRNA-dihydrouridine(16/17) synthase [NAD(P)(+)]-like isoform X3 | -0.516 |
| GB44039 | malate dehydrogenase, cytoplasmic-like isoform 1 | 0.513 |
| GB55781 | LOW QUALITY PROTEIN: uncharacterized protein LOC551170 | -0.513 |
| GB45526 | eukaryotic translation initiation factor 6 isoform 1 | 0.510 |
| GB52789 | 60S ribosomal protein L22 isoform 1 | 0.507 |
| GB53626 | myotrophin-like isoform 2 | 0.507 |
| GB49364 | splicing factor U2af 38 kDa subunit | 0.505 |
| GB44984 | U5 small nuclear ribonucleoprotein 40 kDa protein-like isoform X1 | 0.504 |
| GB50271 | zinc transporter 1-like | 0.503 |
| GB49377 | 40S ribosomal protein S3a | 0.501 |
| GB50874 | transcription factor Ken 2 | -0.501 |
| GB44147 | 60S ribosomal protein L15 | 0.498 |
| GB46141 | LOW QUALITY PROTEIN: vacuolar protein sorting-associated protein 29-like | 0.494 |
| GB51963 | mitochondrial ribonuclease P protein 1 homolog | -0.491 |
| GB55901 | ribosome biogenesis protein NSA2 homolog isoform X1 | 0.488 |
| GB42036 | protein SEC13 homolog isoform X2 | 0.485 |
| GB40877 | translocon-associated protein subunit delta | 0.485 |
| GB44205 | proteasome subunit beta type-5-like | 0.484 |
| GB54151 | uncharacterized protein LOC408463 isoform X12 | -0.484 |
| GB54590 | polyadenylate-binding protein 1-like isoform X2 | 0.483 |
| GB41157 | RPII140-upstream gene protein-like | -0.481 |
| GB48423 | small nuclear ribonucleoprotein F isoform 2 | 0.480 |
| GB49608 | protein angel-like isoform X1 | -0.475 |
| GB49812 | RING-box protein 1A isoform X1 | 0.461 |
| GB43697 | mediator of RNA polymerase II transcription subunit 16 isoform X3 | 0.457 |
| GB41553 | Golgi phosphoprotein 3 homolog rotini-like isoform X1 | 0.455 |
| GB43548 | 40S ribosomal protein SA | 0.449 |
| GB45181 | probable Bax inhibitor 1 | 0.447 |
| GB53086 | alcohol dehydrogenase class-3 isoform X2 | 0.446 |
| GB41724 | uncharacterized protein LOC727081 | -0.446 |
| GB54533 | protein unc-13 homolog D isoform X5 | -0.445 |
| GB40882 | 40S ribosomal protein S13 isoform X1 | 0.445 |
| GB50230 | V-type proton ATPase subunit e 2-like | 0.445 |
| 102654691 | protein translation factor SUI1 homolog | 0.445 |
| GB51787 | myosin light chain alkali-like isoform X5 | 0.444 |
| GB41908 | PERQ amino acid-rich with GYF domain-containing protein CG11148-like isoform X3 | -0.443 |
| GB53138 | inorganic pyrophosphatase-like | 0.437 |
| GB48250 | putative gamma-glutamylcyclotransferase CG2811-like isoform X4 | 0.436 |
| GB46763 | excitatory amino acid transporter 3 | 0.436 |
| GB53415 | WW domain-binding protein 2-like isoform X1 | 0.432 |
| GB47606 | ER membrane protein complex subunit 4-like isoform 1 | 0.431 |
| GB42675 | adenylate cyclase type 2-like | -0.430 |
| GB44312 | hydroxyacylglutathione hydrolase, mitochondrial-like isoform X2 | 0.428 |
| 102654127 | neurochondrin homolog | -0.423 |
| GB47938 | uncharacterized protein LOC412825 isoform X1 | -0.421 |
| GB55056 | spermatogenesis-associated protein 20 isoform X2 | -0.420 |
| GB41084 | 60S ribosomal protein L38 | 0.412 |
| GB47810 | regulator of gene activity protein isoform X3 | 0.410 |
| GB40946 | serine/threonine-protein phosphatase 2A 65 kDa regulatory subunit A alpha isoform-like isoform X1 | 0.409 |
| GB42780 | CCHC-type zinc finger protein CG3800-like isoform X3 | 0.409 |
| GB43229 | GTP-binding nuclear protein Ran isoform X1 | 0.407 |
| GB50244 | NHL repeat-containing protein 2 isoform X4 | -0.406 |
| GB45684 | protein spire-like isoform X4 | -0.406 |
| GB52073 | probable citrate synthase 1, mitochondrial-like | -0.402 |
| GB45856 | protein GPR107-like isoform X4 | 0.401 |
| GB47542 | eukaryotic translation initiation factor 3 subunit J isoform 1 | 0.399 |
| GB53243 | LOW QUALITY PROTEIN: probable phosphorylase b kinase regulatory subunit beta-like | -0.395 |
| GB55892 | glutamate-rich WD repeat-containing protein 1-like | 0.395 |
| GB43105 | casein kinase II subunit alpha isoform X6 | 0.390 |
| GB43537 | probable 28S ribosomal protein S16, mitochondrial | 0.388 |
| GB44496 | probable serine incorporator isoformX1 | 0.376 |
| GB43855 | LOW QUALITY PROTEIN: coatomer subunit beta’ | 0.374 |
| GB40073 | COP9 signalosome complex subunit 8-like | 0.373 |
| GB47100 | putative glutamate synthase [NADPH]-like isoform X4 | -0.372 |
| GB42786 | microtubule-associated protein RP/EB family member 1-like isoform X4 | 0.372 |
| GB54789 | GMP synthase [glutamine-hydrolyzing] | 0.371 |
| GB40767 | phosphoglycolate phosphatase-like | -0.370 |
| GB52212 | polyubiquitin-A-like isoform X2 | 0.370 |
| GB52256 | 60S ribosomal protein L5 | 0.370 |
| GB50925 | prostaglandin E synthase 2-like | -0.360 |
| GB53725 | splicing factor 3B subunit 1-like isoform X2 | -0.355 |
| GB44870 | zinc finger protein 706-like isoform X3 | 0.355 |
| GB45375 | rhomboid-7 isoform X1 | 0.346 |
| GB45044 | uncharacterized protein LOC409396 isoform X5 | -0.334 |
| GB50909 | dual 3’,5’-cyclic-AMP and -GMP phosphodiesterase 11-like, transcript variant X4 | -0.333 |
| GB44907 | myeloid leukemia factor isoform X3 | 0.331 |
| GB44333 | flocculation protein FLO11-like isoform X1 | -0.322 |
| GB46562 | 40S ribosomal protein S24-like isoform X2 | 0.321 |
| GB45017 | RNA pseudouridylate synthase domain-containing protein 2-like isoform X3 | -0.317 |
| GB48312 | pre-mRNA-splicing factor RBM22-like | 0.316 |
| GB47103 | elongation factor 1-beta’ | 0.310 |
| GB48207 | proteasomal ubiquitin receptor ADRM1 homolog isoform X1 | 0.270 |
| GB40887 | V-type proton ATPase subunit E isoform 3 | 0.266 |
| GB41152 | uncharacterized protein C6orf106 homolog | 0.213 |
| GB45678 | 1-acylglycerol-3-phosphate O-acyltransferase ABHD5-like isoform X1 | -0.192 |
| GB44576 | ester hydrolase C11orf54 homolog | 0.189 |
Table S3: The single differentially expressed gene (EBseq; p < 10-5) in Bombus terrestris. Positive fold change values indicate higher expression in the control, while negative values indicate higher expression in the queen pheromone treatment. The second and third columns give the best BLAST hit for this gene in A. mellifera plus the name of the A. mellifera putative ortholog.
kable(bombus.de, "html") %>%
kable_styling()
| Gene | Apis BLAST | Name | Log2 FC |
|---|---|---|---|
| 100648170 | GB48391 | mucin-2-like | 1.071 |
Table S4: List of the 290 significantly differentially expressed genes (EBseq; p < 10-5) in Lasius flavus, listed in order of fold change in gene expression on a Log\(_2\) scale. Positive fold change values indicate higher expression in the control, while negative values indicate higher expression in the queen pheromone treatment. The second and third columns give the best BLAST hit for this gene in A. mellifera plus the name of the A. mellifera putative ortholog.
kable.table(flavus.de)
| Gene | Apis BLAST | Name | Log2 FC |
|---|---|---|---|
| TRINITY_DN19074_c0_g2 | GB43902 | hexaprenyldihydroxybenzoate methyltransferase, mitochondrial-like | 7.514 |
| TRINITY_DN2701_c0_g1 | GB52729 | aspartate–tRNA ligase, cytoplasmic | 7.481 |
| TRINITY_DN14108_c0_g2 | 7.468 | ||
| TRINITY_DN36041_c0_g1 | 6.629 | ||
| TRINITY_DN13621_c0_g1 | 6.549 | ||
| TRINITY_DN18780_c0_g2 | -6.440 | ||
| TRINITY_DN14430_c0_g1 | 6.278 | ||
| TRINITY_DN32671_c0_g2 | 6.121 | ||
| TRINITY_DN14910_c0_g1 | XP_016769216.1 | 5.800 | |
| TRINITY_DN19071_c0_g1 | -5.776 | ||
| TRINITY_DN5663_c0_g2 | XP_006568418.2 | -5.365 | |
| TRINITY_DN13527_c1_g3 | 5.259 | ||
| TRINITY_DN2506_c0_g2 | 5.133 | ||
| TRINITY_DN9902_c0_g2 | 5.069 | ||
| TRINITY_DN6503_c0_g3 | 551397 | 28S ribosomal protein S18a, mitochondrial isoform 2 | 5.044 |
| TRINITY_DN10699_c0_g1 | 4.901 | ||
| TRINITY_DN5102_c0_g1 | XP_016771437.1 | 4.901 | |
| TRINITY_DN6994_c0_g1 | 4.859 | ||
| TRINITY_DN13376_c3_g2 | 4.858 | ||
| TRINITY_DN9565_c0_g3 | GB45250 | uncharacterized protein LOC409595 | 4.811 |
| TRINITY_DN1013_c0_g1 | GB52059 | eukaryotic translation initiation factor 4H-like isoform X1 | 4.709 |
| TRINITY_DN11616_c0_g1 | 4.696 | ||
| TRINITY_DN1845_c0_g2 | GB52253 | protein PRRC2C-like isoform X2 | 4.658 |
| TRINITY_DN7242_c0_g1 | -4.646 | ||
| TRINITY_DN31547_c0_g3 | 4.613 | ||
| TRINITY_DN13376_c3_g3 | 4.569 | ||
| TRINITY_DN6298_c0_g3 | 4.553 | ||
| TRINITY_DN2720_c0_g2 | -4.522 | ||
| TRINITY_DN2583_c0_g2 | 4.460 | ||
| TRINITY_DN24980_c0_g3 | -4.393 | ||
| TRINITY_DN12959_c0_g3 | 4.390 | ||
| TRINITY_DN4813_c0_g1 | 4.322 | ||
| TRINITY_DN6331_c0_g2 | 4.303 | ||
| TRINITY_DN10925_c0_g1 | 4.278 | ||
| TRINITY_DN14174_c1_g3 | 4.233 | ||
| TRINITY_DN23574_c0_g3 | 4.173 | ||
| TRINITY_DN6054_c0_g1 | XP_016771772.1 | 4.143 | |
| TRINITY_DN32287_c0_g1 | 4.133 | ||
| TRINITY_DN1060_c0_g1 | 4.115 | ||
| TRINITY_DN6965_c0_g3 | 4.097 | ||
| TRINITY_DN5087_c0_g1 | XP_003249576.2 | 4.069 | |
| TRINITY_DN10904_c0_g1 | 4.050 | ||
| TRINITY_DN4900_c0_g1 | 4.049 | ||
| TRINITY_DN14065_c0_g2 | 4.015 | ||
| TRINITY_DN2102_c0_g6 | GB40389 | profilin | 3.751 |
| TRINITY_DN12195_c1_g3 | 102656074 | reticulon-4-like isoform X6 | 3.710 |
| TRINITY_DN2302_c0_g2 | 3.676 | ||
| TRINITY_DN9563_c1_g3 | XP_016770117.1 | 3.347 | |
| TRINITY_DN11562_c2_g1 | XP_016769630.1 | 3.211 | |
| TRINITY_DN6503_c0_g2 | 551397 | 28S ribosomal protein S18a, mitochondrial isoform 2 | 3.210 |
| TRINITY_DN3428_c0_g1 | GB53155 | maternal embryonic leucine zipper kinase-like | 3.168 |
| TRINITY_DN11833_c0_g2 | 3.162 | ||
| TRINITY_DN1150_c0_g2 | 3.151 | ||
| TRINITY_DN14156_c9_g2 | XP_016769763.1 | 3.146 | |
| TRINITY_DN7447_c0_g1 | GB10293 | aubergine | 3.125 |
| TRINITY_DN12563_c0_g2 | XP_016768561.1 | 3.097 | |
| TRINITY_DN19328_c0_g2 | GB49105 | ecdysteroid-regulated gene E74 isoform X10 | 2.921 |
| TRINITY_DN19071_c0_g5 | -2.920 | ||
| TRINITY_DN3355_c0_g1 | XP_016772030.1 | 2.912 | |
| TRINITY_DN1453_c0_g2 | 2.891 | ||
| TRINITY_DN34334_c0_g1 | -2.831 | ||
| TRINITY_DN9365_c0_g1 | 2.823 | ||
| TRINITY_DN2907_c0_g1 | GB52114 | protein trachealess-like isoform X7 | 2.821 |
| TRINITY_DN29060_c0_g1 | 2.784 | ||
| TRINITY_DN5450_c0_g3 | 2.778 | ||
| TRINITY_DN6679_c1_g1 | -2.777 | ||
| TRINITY_DN13106_c0_g1 | -2.766 | ||
| TRINITY_DN6249_c0_g2 | 2.762 | ||
| TRINITY_DN12570_c0_g2 | XP_016772046.1 | 2.752 | |
| TRINITY_DN29060_c0_g2 | -2.748 | ||
| TRINITY_DN1453_c0_g1 | 2.718 | ||
| TRINITY_DN4551_c0_g1 | 2.665 | ||
| TRINITY_DN5934_c0_g2 | 2.664 | ||
| TRINITY_DN21319_c0_g1 | 2.647 | ||
| TRINITY_DN16415_c0_g2 | 2.644 | ||
| TRINITY_DN6639_c0_g2 | GB51740 | CD63 antigen | 2.628 |
| TRINITY_DN8686_c0_g6 | 2.525 | ||
| TRINITY_DN27412_c0_g1 | 2.511 | ||
| TRINITY_DN7556_c0_g1 | 2.479 | ||
| TRINITY_DN12097_c3_g11 | 2.467 | ||
| TRINITY_DN19324_c0_g1 | 2.464 | ||
| TRINITY_DN5257_c0_g2 | GB51614 | probable methylthioribulose-1-phosphate dehydratase-like | 2.451 |
| TRINITY_DN3033_c0_g1 | GB47735 | endonuclease III-like protein 1-like | 2.441 |
| TRINITY_DN23065_c0_g1 | 2.434 | ||
| TRINITY_DN30835_c0_g2 | 2.337 | ||
| TRINITY_DN30278_c0_g7 | 2.328 | ||
| TRINITY_DN13221_c0_g7 | 2.244 | ||
| TRINITY_DN13083_c0_g1 | 2.202 | ||
| TRINITY_DN12097_c3_g6 | 2.167 | ||
| TRINITY_DN6372_c0_g3 | 2.154 | ||
| TRINITY_DN13237_c2_g6 | -2.137 | ||
| TRINITY_DN3870_c0_g2 | 2.108 | ||
| TRINITY_DN7016_c0_g2 | GB47843 | uncharacterized protein LOC100576559 isoform X2 | 1.972 |
| TRINITY_DN12195_c1_g4 | 102656074 | reticulon-4-like isoform X6 | -1.727 |
| TRINITY_DN15459_c0_g1 | 1.644 | ||
| TRINITY_DN7587_c0_g2 | GB52590 | fatty acid synthase-like isoform 1 | -1.363 |
| TRINITY_DN3266_c0_g1 | 1.320 | ||
| TRINITY_DN5353_c0_g1 | GB43825 | lysosomal aspartic protease | 1.297 |
| TRINITY_DN7865_c0_g1 | XP_016770671.1 | 1.257 | |
| TRINITY_DN13667_c2_g1 | 1.226 | ||
| TRINITY_DN9568_c0_g3 | -1.068 | ||
| TRINITY_DN8668_c0_g1 | GB52590 | fatty acid synthase-like isoform 1 | -1.025 |
| TRINITY_DN8075_c0_g1 | -1.023 | ||
| TRINITY_DN8944_c1_g2 | -0.955 | ||
| TRINITY_DN13195_c1_g2 | 0.950 | ||
| TRINITY_DN11726_c1_g1 | GB52590 | fatty acid synthase-like isoform 1 | -0.932 |
| TRINITY_DN14247_c8_g2 | GB52590 | fatty acid synthase-like isoform 1 | -0.926 |
| TRINITY_DN61_c0_g1 | GB45775 | pancreatic triacylglycerol lipase-like isoform X2 | -0.888 |
| TRINITY_DN2623_c0_g1 | GB43825 | lysosomal aspartic protease | 0.862 |
| TRINITY_DN12575_c0_g1 | GB55263 | putative fatty acyl-CoA reductase CG5065-like | -0.832 |
| TRINITY_DN14020_c0_g1 | GB46188 | trichohyalin-like isoform X1 | 0.728 |
| TRINITY_DN13013_c0_g1 | XP_016768441.1 | 0.710 | |
| TRINITY_DN12756_c2_g1 | 0.691 | ||
| TRINITY_DN9649_c0_g1 | NP_001305411.1 | 0.685 | |
| TRINITY_DN13574_c1_g2 | GB40681 | elongation of very long chain fatty acids protein 1-like | -0.679 |
| TRINITY_DN9287_c0_g1 | XP_016768964.1 | 0.671 | |
| TRINITY_DN13318_c0_g1 | GB46888 | alpha-methylacyl-CoA racemase-like | -0.612 |
| TRINITY_DN3111_c0_g1 | 0.588 | ||
| TRINITY_DN13226_c0_g1 | GB47475 | protein lethal(2)essential for life-like isoform 1 | 0.586 |
| TRINITY_DN5134_c0_g1 | XP_016770229.1 | 0.578 | |
| TRINITY_DN12647_c0_g1 | XP_016773029.1 | -0.572 | |
| TRINITY_DN14059_c0_g1 | XP_016768888.1 | 0.567 | |
| TRINITY_DN13252_c1_g1 | GB50415 | diacylglycerol kinase theta-like isoform X7 | 0.559 |
| TRINITY_DN13742_c0_g1 | GB46657 | galactokinase-like | -0.518 |
| TRINITY_DN13982_c0_g1 | XP_016769706.1 | -0.517 | |
| TRINITY_DN32324_c0_g1 | 102656101 | uncharacterized protein LOC102656101 | 0.517 |
| TRINITY_DN12496_c0_g1 | GB54423 | uncharacterized protein LOC551958 | 0.511 |
| TRINITY_DN11328_c0_g1 | GB51479 | ras guanine nucleotide exchange factor P-like isoform X3 | 0.509 |
| TRINITY_DN6523_c0_g1 | GB40976 | heat shock protein 90 | -0.504 |
| TRINITY_DN12344_c0_g1 | 0.503 | ||
| TRINITY_DN15124_c0_g1 | 0.500 | ||
| TRINITY_DN12742_c1_g1 | XP_016767680.1 | 0.490 | |
| TRINITY_DN11193_c0_g1 | GB53045 | ATP-binding cassette sub-family G member 1-like isoform X1 | -0.481 |
| TRINITY_DN10448_c0_g2 | GB41603 | PTB domain-containing adapter protein ced-6 isoform X2 | -0.474 |
| TRINITY_DN1154_c0_g1 | 0.474 | ||
| TRINITY_DN14164_c3_g1 | GB55490 | uncharacterized protein LOC410793 | -0.473 |
| TRINITY_DN14136_c5_g1 | GB55016 | quinone oxidoreductase-like isoform X2 | 0.465 |
| TRINITY_DN9952_c0_g1 | GB43823 | chemosensory protein 1 precursor | 0.462 |
| TRINITY_DN8450_c0_g1 | GB46286 | zinc carboxypeptidase A 1-like isoform X1 | 0.454 |
| TRINITY_DN12807_c0_g1 | XP_016769434.1 | 0.450 | |
| TRINITY_DN13250_c5_g1 | GB45937 | intracellular protein transport protein USO1 isoform X2 | 0.445 |
| TRINITY_DN6544_c0_g1 | GB52074 | 6-phosphogluconate dehydrogenase, decarboxylating | -0.445 |
| TRINITY_DN13581_c2_g2 | GB42792 | uncharacterized protein LOC409805 isoform X3 | 0.444 |
| TRINITY_DN36181_c0_g1 | 0.442 | ||
| TRINITY_DN2719_c0_g1 | GB54446 | arginine kinase isoform X2 | 0.441 |
| TRINITY_DN13519_c0_g1 | GB42797 | protein takeout-like | 0.440 |
| TRINITY_DN7060_c0_g1 | GB49607 | lysosome-associated membrane glycoprotein 1-like isoform 2 | -0.438 |
| TRINITY_DN1392_c0_g1 | GB44205 | proteasome subunit beta type-5-like | -0.434 |
| TRINITY_DN10466_c0_g1 | GB44431 | 26S protease regulatory subunit 4 isoform 1 | -0.428 |
| TRINITY_DN13148_c0_g1 | GB44213 | filamin-like | 0.426 |
| TRINITY_DN13702_c3_g1 | XP_016769732.1 | 0.423 | |
| TRINITY_DN12417_c0_g2 | GB45456 | flocculation protein FLO11-like isoform X2 | 0.422 |
| TRINITY_DN23399_c0_g1 | 0.417 | ||
| TRINITY_DN11737_c0_g1 | XP_016766478.1 | -0.416 | |
| TRINITY_DN12348_c0_g1 | GB44703 | proteasome activator complex subunit 4-like | -0.415 |
| TRINITY_DN13581_c1_g3 | XP_016767189.1 | 0.406 | |
| TRINITY_DN11774_c0_g1 | XP_016772498.1 | 0.387 | |
| TRINITY_DN3048_c0_g1 | GB40770 | dehydrogenase/reductase SDR family member 11-like isoform X2 | 0.387 |
| TRINITY_DN13700_c5_g3 | GB42840 | leukocyte receptor cluster member 8 homolog isoform X4 | 0.387 |
| TRINITY_DN13455_c0_g1 | GB45128 | trifunctional enzyme subunit alpha, mitochondrial-like | -0.380 |
| TRINITY_DN14019_c2_g1 | 409060 | neurofilament heavy polypeptide-like isoform X2 | 0.377 |
| TRINITY_DN11786_c1_g1 | GB51214 | troponin T, skeletal muscle | 0.374 |
| TRINITY_DN9982_c0_g1 | GB51787 | myosin light chain alkali-like isoform X5 | 0.372 |
| TRINITY_DN27322_c0_g1 | GB40866 | heat shock protein cognate 4 | -0.369 |
| TRINITY_DN5956_c0_g1 | 0.366 | ||
| TRINITY_DN6208_c0_g1 | GB49757 | fatty acid binding protein | 0.359 |
| TRINITY_DN11594_c0_g1 | GB52643 | poly(U)-specific endoribonuclease homolog | 0.355 |
| TRINITY_DN9687_c0_g1 | 0.350 | ||
| TRINITY_DN14119_c3_g1 | 726668 | PDZ and LIM domain protein 3 isoform X7 | 0.348 |
| TRINITY_DN5256_c0_g1 | 0.345 | ||
| TRINITY_DN10396_c0_g1 | GB42607 | cytochrome b5-like isoform X1 | -0.344 |
| TRINITY_DN5623_c0_g1 | GB54817 | muscle-specific protein 20 | 0.343 |
| TRINITY_DN10620_c0_g1 | GB42732 | long-chain-fatty-acid–CoA ligase 3-like isoform X2 | -0.325 |
| TRINITY_DN12788_c0_g1 | XP_016771468.1 | 0.325 | |
| TRINITY_DN12757_c0_g1 | GB55610 | MOSC domain-containing protein 2, mitochondrial-like | 0.324 |
| TRINITY_DN10923_c0_g1 | GB40141 | venom serine carboxypeptidase | -0.321 |
| TRINITY_DN10232_c0_g1 | -0.319 | ||
| TRINITY_DN12105_c0_g1 | XP_016768441.1 | 0.318 | |
| TRINITY_DN7549_c0_g1 | XP_016768456.1 | 0.315 | |
| TRINITY_DN3036_c0_g1 | GB52326 | chemosensory protein 4 precursor | 0.313 |
| TRINITY_DN12756_c2_g4 | XP_016770894.1 | 0.311 | |
| TRINITY_DN14002_c3_g1 | XP_016770982.1 | 0.307 | |
| TRINITY_DN27284_c0_g1 | GB50274 | transitional endoplasmic reticulum ATPase TER94 | -0.306 |
| TRINITY_DN12138_c0_g1 | GB47306 | sulfhydryl oxidase 1-like | 0.305 |
| TRINITY_DN13865_c0_g1 | GB47963 | probable E3 ubiquitin-protein ligase HERC4-like isoform X3 | 0.302 |
| TRINITY_DN8423_c0_g1 | XP_016768214.1 | -0.298 | |
| TRINITY_DN27569_c0_g1 | GB52736 | ATP synthase subunit beta, mitochondrial isoform X1 | 0.297 |
| TRINITY_DN14286_c2_g1 | GB54861 | LOW QUALITY PROTEIN: counting factor associated protein D-like | -0.294 |
| TRINITY_DN14128_c1_g1 | XP_006568818.2 | 0.291 | |
| TRINITY_DN11359_c0_g1 | XP_016768872.1 | -0.287 | |
| TRINITY_DN9072_c0_g1 | XP_016768321.1 | -0.287 | |
| TRINITY_DN28113_c0_g1 | -0.285 | ||
| TRINITY_DN10911_c0_g1 | XP_016770213.1 | -0.277 | |
| TRINITY_DN12726_c3_g1 | GB42787 | dentin sialophosphoprotein-like isoform X4 | -0.274 |
| TRINITY_DN6072_c0_g1 | XP_016771431.1 | -0.273 | |
| TRINITY_DN13789_c0_g2 | XP_016767109.1 | 0.273 | |
| TRINITY_DN14037_c0_g1 | XP_016767155.1 | 0.272 | |
| TRINITY_DN13738_c0_g1 | XP_016772667.1 | 0.271 | |
| TRINITY_DN993_c0_g3 | 0.270 | ||
| TRINITY_DN7531_c0_g3 | GB51710 | eukaryotic initiation factor 4A-like isoformX2 | 0.260 |
| TRINITY_DN11232_c0_g1 | GB40240 | myosin regulatory light chain 2 | 0.258 |
| TRINITY_DN12074_c1_g1 | GB47462 | protein disulfide-isomerase A3 isoform 2 | -0.256 |
| TRINITY_DN11684_c0_g1 | GB55537 | transketolase isoform 1 | -0.248 |
| TRINITY_DN14138_c2_g1 | GB48850 | fatty-acid amide hydrolase 2-B-like | -0.248 |
| TRINITY_DN13963_c1_g1 | XP_016768450.1 | 0.247 | |
| TRINITY_DN12180_c0_g1 | XP_016772046.1 | 0.246 | |
| TRINITY_DN13233_c1_g1 | XP_016768217.1 | -0.244 | |
| TRINITY_DN12080_c1_g1 | XP_016769481.1 | -0.241 | |
| TRINITY_DN11171_c0_g1 | GB42468 | phospholipase B1, membrane-associated-like isoform X1 | -0.239 |
| TRINITY_DN13982_c0_g3 | XP_016769706.1 | -0.237 | |
| TRINITY_DN14752_c0_g1 | GB50123 | myophilin-like | 0.226 |
| TRINITY_DN8270_c0_g1 | GB43276 | aminopeptidase N-like isoform X1 | 0.226 |
| TRINITY_DN12844_c1_g1 | GB47885 | probable cytochrome P450 304a1 | -0.224 |
| TRINITY_DN11885_c1_g1 | GB55598 | troponin I isoform X23 | 0.218 |
| TRINITY_DN8742_c0_g1 | XP_016767150.1 | -0.216 | |
| TRINITY_DN14111_c0_g1 | GB46705 | muscle M-line assembly protein unc-89 isoform X5 | 0.213 |
| TRINITY_DN14002_c4_g1 | 0.212 | ||
| TRINITY_DN7802_c0_g1 | GB41358 | elongation factor 1-alpha | -0.210 |
| TRINITY_DN14006_c0_g1 | XP_016767101.1 | -0.208 | |
| TRINITY_DN8847_c0_g1 | GB46772 | very-long-chain enoyl-CoA reductase-like | -0.201 |
| TRINITY_DN14179_c1_g1 | GB40461 | calreticulin | -0.186 |
| TRINITY_DN7523_c0_g1 | -0.183 | ||
| TRINITY_DN12909_c0_g1 | XP_016770377.1 | 0.181 | |
| TRINITY_DN8174_c0_g1 | GB47880 | superoxide dismutase 1 | -0.175 |
| TRINITY_DN14199_c2_g1 | -0.173 | ||
| TRINITY_DN3676_c0_g2 | GB49773 | sequestosome-1 | 0.168 |
| TRINITY_DN3648_c0_g1 | GB45181 | probable Bax inhibitor 1 | -0.167 |
| TRINITY_DN9738_c0_g1 | GB44206 | death-associated protein 1-like | -0.167 |
| TRINITY_DN3697_c0_g1 | GB54368 | prostaglandin E synthase 3-like isoform X2 | -0.165 |
| TRINITY_DN13223_c0_g1 | GB54315 | uncharacterized protein LOC724126 | -0.157 |
| TRINITY_DN9957_c0_g1 | GB43831 | ATP-binding cassette sub-family D member 3-like | -0.157 |
| TRINITY_DN1533_c0_g1 | XP_392401.3 | -0.155 | |
| TRINITY_DN12307_c0_g1 | GB47029 | uncharacterized protein LOC724558 | -0.153 |
| TRINITY_DN13021_c0_g1 | XP_006571535.2 | -0.144 | |
| TRINITY_DN11571_c0_g2 | XP_001119981.3 | -0.138 | |
| TRINITY_DN14152_c0_g10 | XP_016771978.1 | 0.136 | |
| TRINITY_DN13002_c1_g1 | XP_016767675.1 | -0.131 | |
| TRINITY_DN13997_c1_g2 | XP_016771269.1 | 0.130 | |
| TRINITY_DN7931_c0_g1 | GB49321 | D-arabinitol dehydrogenase 1-like | -0.128 |
| TRINITY_DN12756_c2_g5 | XP_016770894.1 | -0.126 | |
| TRINITY_DN1575_c0_g1 | 0.124 | ||
| TRINITY_DN1616_c0_g1 | GB41545 | MD-2-related lipid-recognition protein-like | 0.120 |
| TRINITY_DN12630_c0_g1 | GB45258 | isocitrate dehydrogenase [NADP] cytoplasmic isoform 2 | -0.119 |
| TRINITY_DN14083_c3_g1 | GB55263 | putative fatty acyl-CoA reductase CG5065-like | -0.117 |
| TRINITY_DN4494_c0_g2 | GB47990 | tropomyosin-1-like | 0.116 |
| TRINITY_DN1524_c0_g1 | GB46920 | iron-sulfur cluster assembly enzyme ISCU, mitochondrial | 0.115 |
| TRINITY_DN13221_c0_g9 | XP_016769341.1 | 0.107 | |
| TRINITY_DN13959_c2_g1 | GB49688 | peroxidase isoformX2 | 0.104 |
| TRINITY_DN12634_c0_g1 | GB43575 | trehalase-like isoform X2 | -0.093 |
| TRINITY_DN13844_c1_g1 | XP_016767538.1 | -0.092 | |
| TRINITY_DN10322_c0_g1 | XP_016769014.1 | -0.088 | |
| TRINITY_DN13381_c0_g1 | GB51633 | protein HIRA homolog | 0.084 |
| TRINITY_DN12970_c0_g2 | GB44208 | WD repeat-containing protein 37-like isoform X4 | 0.083 |
| TRINITY_DN3647_c0_g1 | GB53550 | heat shock protein beta-1-like isoform X3 | -0.081 |
| TRINITY_DN8558_c0_g1 | GB46713 | translation elongation factor 2-like isoform 1 | -0.079 |
| TRINITY_DN11372_c0_g1 | GB53755 | juvenile hormone esterase precursor | 0.071 |
| TRINITY_DN6049_c0_g1 | 0.068 | ||
| TRINITY_DN10813_c0_g1 | GB51753 | uncharacterized protein LOC100576760 isoform X2 | -0.066 |
| TRINITY_DN10427_c0_g1 | GB51782 | carboxypeptidase Q-like isoform 1 | -0.065 |
| TRINITY_DN8685_c0_g4 | GB43825 | lysosomal aspartic protease | -0.065 |
| TRINITY_DN13047_c0_g1 | XP_016768229.1 | 0.061 | |
| TRINITY_DN6208_c0_g2 | GB49757 | fatty acid binding protein | -0.056 |
| TRINITY_DN13652_c0_g1 | GB42422 | ADP/ATP translocase | 0.054 |
| TRINITY_DN13884_c0_g2 | GB47405 | neutral alpha-glucosidase AB-like isoform 2 | 0.051 |
| TRINITY_DN13634_c0_g1 | GB45913 | protein lethal(2)essential for life-like | -0.049 |
| TRINITY_DN1723_c0_g1 | GB52324 | chemosensory protein 3 precursor | 0.048 |
| TRINITY_DN18895_c0_g1 | GB55581 | membrane-associated progesterone receptor component 1-like isoform 2 | -0.044 |
| TRINITY_DN8126_c0_g1 | GB40779 | transaldolase | -0.044 |
| TRINITY_DN10665_c0_g1 | GB42829 | juvenile hormone epoxide hydrolase 1 | -0.042 |
| TRINITY_DN8184_c0_g1 | 0.040 | ||
| TRINITY_DN11577_c0_g1 | GB55096 | NADP-dependent malic enzyme isoform X3 | 0.040 |
| TRINITY_DN18992_c0_g1 | XP_016772082.1 | 0.039 | |
| TRINITY_DN11030_c0_g1 | GB49240 | aldehyde dehydrogenase, mitochondrial isoform 1 | -0.038 |
| TRINITY_DN11459_c0_g1 | GB50598 | aldose reductase-like isoform 1 | -0.038 |
| TRINITY_DN13961_c1_g3 | GB52588 | conserved oligomeric Golgi complex subunit 7 | -0.037 |
| TRINITY_DN12872_c0_g1 | GB53333 | V-type proton ATPase catalytic subunit A-like isoform X3 | 0.035 |
| TRINITY_DN13271_c0_g1 | GB40312 | choline/ethanolamine kinase-like isoform X4 | 0.030 |
| TRINITY_DN13702_c8_g1 | GB47395 | uncharacterized protein CG7816-like | -0.030 |
| TRINITY_DN13400_c0_g1 | GB54421 | uncharacterized protein DDB_G0287625-like | 0.023 |
| TRINITY_DN10682_c0_g1 | GB50252 | GTP-binding protein SAR1b-like isoform X4 | -0.021 |
| TRINITY_DN8055_c0_g1 | -0.021 | ||
| TRINITY_DN9151_c0_g1 | GB45147 | clavesin-2-like | 0.021 |
| TRINITY_DN11885_c3_g1 | GB47880 | superoxide dismutase 1 | -0.019 |
| TRINITY_DN12979_c1_g1 | GB49347 | prostaglandin reductase 1-like | 0.013 |
| TRINITY_DN14085_c1_g1 | XP_016769919.1 | -0.011 | |
| TRINITY_DN11118_c1_g1 | GB44422 | uncharacterized protein LOC412543 isoform X3 | -0.010 |
| TRINITY_DN14002_c1_g1 | 0.004 | ||
| TRINITY_DN7306_c0_g2 | XP_016769332.1 | -0.004 | |
| TRINITY_DN13747_c0_g1 | XP_016769944.1 | -0.003 | |
| TRINITY_DN10790_c0_g1 | 0.000 |
Table S5: List of the 135 significantly differentially expressed genes (EBseq; p < 10-5) in Lasius niger, listed in order of fold change in gene expression on a Log\(_2\) scale. Positive fold change values indicate higher expression in the control, while negative values indicate higher expression in the queen pheromone treatment. The second and third columns give the best BLAST hit for this gene in A. mellifera plus the name of the A. mellifera putative ortholog.
kable.table(niger.de)
| Gene | Apis BLAST | Name | Log2 FC |
|---|---|---|---|
| XLOC_001009 | 5.916 | ||
| RF55_9944 | GB55171 | major royal jelly protein 1 isoform X1 | 5.060 |
| RF55_873 | XP_016773511.1 | 4.638 | |
| XLOC_000784 | 3.626 | ||
| RF55_874 | XP_016766165.1 | 3.550 | |
| XLOC_016588 | 3.077 | ||
| RF55_9436 | 2.813 | ||
| RF55_3510 | GB53672 | failed axon connections isoform X2 | -2.471 |
| RF55_15864 | -2.439 | ||
| XLOC_020552 | 2.437 | ||
| RF55_783 | 2.206 | ||
| RF55_6001 | -2.150 | ||
| XLOC_013573 | 2.150 | ||
| RF55_4870 | XP_006563262.2 | -2.031 | |
| XLOC_022706 | -1.091 | ||
| RF55_7689 | XP_003250465.2 | -1.030 | |
| RF55_19841 | GB52590 | fatty acid synthase-like isoform 1 | -1.015 |
| RF55_21338 | GB52590 | fatty acid synthase-like isoform 1 | -0.923 |
| RF55_13568 | XP_006571191.2 | 0.882 | |
| RF55_2210 | GB49869 | microsomal triglyceride transfer protein large subunit isoform X1 | -0.879 |
| RF55_6639 | GB48784 | cytochrome c | 0.779 |
| RF55_15245 | GB43617 | uncharacterized membrane protein DDB_G0293934-like isoform X1 | 0.734 |
| RF55_14443 | GB51356 | cytochrome P450 4G11 | 0.726 |
| RF55_5140 | XP_016767978.1 | 0.656 | |
| XLOC_003947 | 0.655 | ||
| XLOC_019296 | -0.643 | ||
| XLOC_005895 | -0.625 | ||
| XLOC_010120 | 0.619 | ||
| RF55_3431 | GB47849 | pyrroline-5-carboxylate reductase 2-like isoform X2 | 0.611 |
| RF55_6542 | GB52074 | 6-phosphogluconate dehydrogenase, decarboxylating | -0.603 |
| RF55_6567 | 552211 | protein THEM6-like | -0.597 |
| RF55_11093 | GB51174 | uncharacterized protein DDB_G0284459-like | 0.593 |
| RF55_9960 | GB52023 | cytochrome P450 6AQ1 isoform X3 | -0.584 |
| RF55_14139 | XP_016768457.1 | 0.561 | |
| RF55_16317 | XP_016770827.1 | -0.523 | |
| RF55_16054 | GB55082 | protein PBDC1-like | 0.489 |
| XLOC_004490 | -0.474 | ||
| RF55_9918 | GB47885 | probable cytochrome P450 304a1 | 0.470 |
| XLOC_015751 | -0.442 | ||
| RF55_12610 | GB40866 | heat shock protein cognate 4 | -0.432 |
| RF55_11067 | GB46772 | very-long-chain enoyl-CoA reductase-like | -0.431 |
| RF55_6451 | GB55598 | troponin I isoform X23 | 0.430 |
| RF55_10641 | XP_016769078.1 | -0.430 | |
| RF55_4656 | GB42792 | uncharacterized protein LOC409805 isoform X3 | 0.415 |
| RF55_4036 | GB44208 | WD repeat-containing protein 37-like isoform X4 | 0.407 |
| XLOC_002901 | -0.398 | ||
| RF55_16927 | XP_006564499.2 | 0.394 | |
| RF55_4554 | GB47990 | tropomyosin-1-like | 0.393 |
| RF55_15079 | GB41028 | ATP synthase subunit alpha, mitochondrial isoform 1 | 0.375 |
| RF55_3507 | GB41333 | DNA-directed RNA polymerase III subunit RPC1-like isoform X1 | -0.375 |
| RF55_5177 | GB43902 | hexaprenyldihydroxybenzoate methyltransferase, mitochondrial-like | -0.368 |
| RF55_13988 | GB55263 | putative fatty acyl-CoA reductase CG5065-like | -0.362 |
| RF55_10649 | 0.359 | ||
| RF55_2038 | GB51787 | myosin light chain alkali-like isoform X5 | 0.350 |
| RF55_3707 | GB55537 | transketolase isoform 1 | -0.342 |
| XLOC_005759 | 0.330 | ||
| RF55_10912 | GB47880 | superoxide dismutase 1 | -0.324 |
| RF55_18605 | XP_016770827.1 | -0.315 | |
| RF55_17057 | GB52590 | fatty acid synthase-like isoform 1 | -0.312 |
| RF55_3648 | XP_016768682.1 | -0.310 | |
| RF55_5902 | GB55302 | trehalose transporter 1 isoform X6 | 0.308 |
| RF55_12242 | GB41912 | trans-1,2-dihydrobenzene-1,2-diol dehydrogenase-like | -0.286 |
| RF55_10676 | GB40240 | myosin regulatory light chain 2 | 0.279 |
| RF55_4654 | GB45673 | alpha-N-acetylgalactosaminidase-like | 0.277 |
| XLOC_012799 | 0.273 | ||
| XLOC_018477 | -0.268 | ||
| RF55_6754 | XP_016772080.1 | 0.254 | |
| RF55_3967 | GB46039 | tubulin alpha-1 chain-like | -0.251 |
| RF55_1582 | GB45012 | adenosylhomocysteinase-like | 0.248 |
| RF55_2761 | XP_003249233.2 | 0.246 | |
| RF55_2493 | GB45913 | protein lethal(2)essential for life-like | -0.244 |
| RF55_15035 | GB51356 | cytochrome P450 4G11 | -0.223 |
| RF55_5799 | GB50123 | myophilin-like | 0.216 |
| RF55_5341 | GB50508 | fibrillin-2 | -0.215 |
| RF55_598 | GB40021 | probable serine/threonine-protein kinase clkA-like | -0.215 |
| RF55_5109 | XP_016767675.1 | -0.211 | |
| RF55_2407 | XP_016768440.1 | 0.207 | |
| RF55_3343 | GB46290 | acetyl-coenzyme A synthetase-like | -0.205 |
| RF55_10752 | XP_016771487.1 | 0.204 | |
| RF55_19196 | GB41311 | actin, indirect flight muscle-like | 0.202 |
| RF55_5837 | GB43879 | aquaporin AQPcic-like isoform X2 | -0.191 |
| RF55_13604 | XP_016767981.1 | 0.185 | |
| RF55_3994 | GB49175 | 4-hydroxyphenylpyruvate dioxygenase-like | 0.181 |
| RF55_18796 | GB53412 | fatty acid synthase-like | -0.180 |
| XLOC_001770 | 0.175 | ||
| RF55_1934 | GB54827 | synaptotagmin 1 | -0.169 |
| RF55_5219 | GB51753 | uncharacterized protein LOC100576760 isoform X2 | -0.163 |
| RF55_778 | GB42422 | ADP/ATP translocase | 0.154 |
| RF55_10519 | GB54446 | arginine kinase isoform X2 | 0.141 |
| RF55_364 | 0.137 | ||
| RF55_2231 | XP_016773593.1 | -0.134 | |
| XLOC_008839 | -0.132 | ||
| RF55_5431 | -0.129 | ||
| RF55_5198 | XP_016768517.1 | 0.124 | |
| RF55_11370 | XP_016772844.1 | -0.115 | |
| RF55_13251 | GB52590 | fatty acid synthase-like isoform 1 | -0.113 |
| RF55_6842 | GB43052 | paramyosin, long form-like | 0.109 |
| RF55_6077 | GB54423 | uncharacterized protein LOC551958 | -0.108 |
| RF55_6180 | GB40758 | icarapin-like | 0.108 |
| XLOC_005990 | -0.099 | ||
| RF55_10150 | XP_016769706.1 | 0.099 | |
| RF55_1045 | GB54861 | LOW QUALITY PROTEIN: counting factor associated protein D-like | -0.097 |
| RF55_3186 | XP_016770377.1 | 0.092 | |
| XLOC_020265 | -0.089 | ||
| XLOC_019117 | -0.085 | ||
| RF55_4175 | GB44311 | actin related protein 1 | 0.083 |
| XLOC_016272 | -0.079 | ||
| RF55_5206 | GB40735 | fructose-bisphosphate aldolase-like isoform X1 | 0.071 |
| RF55_4024 | XP_016767817.1 | 0.069 | |
| RF55_9453 | GB55096 | NADP-dependent malic enzyme isoform X3 | -0.067 |
| RF55_8355 | GB42809 | translationally-controlled tumor protein homolog isoform 1 | 0.063 |
| RF55_3575 | XP_016768967.1 | -0.062 | |
| XLOC_011290 | 0.061 | ||
| RF55_5559 | GB52107 | tubulin alpha-1 chain-like | 0.061 |
| RF55_3308 | -0.059 | ||
| XLOC_020794 | 0.059 | ||
| XLOC_018966 | 0.059 | ||
| RF55_1104 | XP_016769017.1 | 0.048 | |
| RF55_652 | GB54354 | uncharacterized protein DDB_G0274915-like isoform X2 | 0.045 |
| RF55_3854 | XP_006571125.2 | -0.036 | |
| RF55_6873 | GB47106 | NADH-ubiquinone oxidoreductase 75 kDa subunit, mitochondrial | -0.035 |
| RF55_15158 | GB42794 | circadian clock-controlled protein-like isoform 1 | -0.034 |
| RF55_4888 | GB40779 | transaldolase | 0.034 |
| XLOC_019193 | 0.026 | ||
| XLOC_013126 | -0.025 | ||
| XLOC_017016 | 0.025 | ||
| XLOC_016458 | -0.024 | ||
| XLOC_013131 | -0.013 | ||
| RF55_10886 | GB41427 | catalase | -0.012 |
| XLOC_003165 | -0.010 | ||
| RF55_9333 | GB49688 | peroxidase isoformX2 | 0.008 |
| XLOC_004885 | -0.005 | ||
| RF55_5677 | GB46713 | translation elongation factor 2-like isoform 1 | 0.004 |
| RF55_14822 | GB43823 | chemosensory protein 1 precursor | 0.004 |
| RF55_11002 | XP_016768909.1 | 0.002 |
In the first pair of tables, we have simply listed the genes that showed statistically significant differential expression in two or more species. This method makes few false positives, but it likely misses many of true overlaps because our study has modest power to detect differential expression.
In the third table, we instead look for similarities between species using a method that ranks genes from most- to least- phermone sensitive based on log fold change, alleviating the problem of . To do this, we select the top n genes per species (where n = 100, 200 … 500), based on the absolute magnitude of the log fold-change response to queen pheromone, giving a list of the most pheromone-sensitive genes. We beleive that this alternative method likely produces fewer false negatives in our search for overlapping genes, at cost of getting more false positives.
# Define a function to test whether the overlap of two sets of differentially expressed genes,
# drawn from a common pool (e.g. all the orthologs that were tested), is higher or lower than expected
# Inspiration for this code: https://stats.stackexchange.com/questions/10328/using-rs-phyper-to-get-the-probability-of-list-overlap
overlap.hypergeometric.test <- function(n.overlaps, num.sig1, num.sig2, num.genes, species){
p.smaller <- phyper(n.overlaps, num.sig1, num.genes - num.sig1, num.sig2)
p.higher <- 1 - phyper(n.overlaps - 1, num.sig1, num.genes - num.sig1, num.sig2)
output <- data.frame(Species = species,
Test = c("Overlap is lower than expected:",
"Overlap is higher than expected:"),
p = c(p.smaller, p.higher))
output[output$p == min(output$p), ]
}
# Apis and flavus
af.oggs <- make.OGGs(c("am", "lf"))[[2]] # Get the orthologous gene list
n.am <- (tbl(my_db, "ebseq_padj_gene_am") %>%
filter(gene %in% af.oggs$am) %>%
summarise(n=n()) %>%
as.data.frame())[1,1] # Count the number of diff expressed genes that appear in the OGG list
n.lf <- (tbl(my_db, "ebseq_padj_gene_lf") %>%
filter(gene %in% af.oggs$lf) %>% summarise(n=n()) %>%
as.data.frame())[1,1]
num.oggs.af <- nrow(af.oggs) # Count the orthologous genes
af.oggs <- suppressMessages(
af.oggs %>%
filter(am %in% (tbl(my_db, "ebseq_padj_gene_am") %>%
as.data.frame())[,1],
lf %in% (tbl(my_db, "ebseq_padj_gene_lf") %>%
as.data.frame())[,1]) %>%
mutate(Species = "Apis and L. flavus") %>%
left_join(tbl(my_db, "ebseq_gene_am") %>%
select(gene, PostFC) %>%
rename(am=gene), copy=T) %>%
rename(`Apis FC` = PostFC) %>%
left_join(tbl(my_db, "ebseq_gene_lf") %>%
select(gene, PostFC) %>%
rename(lf=gene), copy=T) %>%
rename(`L. flavus FC` = PostFC) %>%
left_join(tbl(my_db, "bee_names") %>%
rename(am=gene), copy=T))
num.overlap.af <- nrow(af.oggs) # Count the overlaps
test1 <- overlap.hypergeometric.test(num.overlap.af,
n.am, n.lf,
num.oggs.af,
"Apis and L. flavus") # Run the hypergeometric test
# Apis and niger
an.oggs <- make.OGGs(c("am", "ln"))[[2]] # Get the orthologous gene list
n.am <- (tbl(my_db, "ebseq_padj_gene_am") %>%
filter(gene %in% an.oggs$am) %>%
summarise(n=n()) %>% as.data.frame())[1,1] # Count the number of diff expressed genes that appear in the OGG list
n.ln <- (tbl(my_db, "ebseq_padj_gene_ln") %>%
filter(gene %in% an.oggs$ln) %>%
summarise(n=n()) %>% as.data.frame())[1,1]
num.oggs.an <- nrow(an.oggs) # Count the orthologous genes
an.oggs <- suppressMessages(
an.oggs %>%
filter(am %in% (tbl(my_db, "ebseq_padj_gene_am") %>% as.data.frame())[,1],
ln %in% (tbl(my_db, "ebseq_padj_gene_ln") %>% as.data.frame())[,1]) %>%
mutate(Species = "Apis and L. niger") %>%
left_join(tbl(my_db, "ebseq_gene_am") %>%
select(gene, PostFC) %>%
rename(am=gene), copy=T) %>%
rename(`Apis FC` = PostFC) %>%
left_join(tbl(my_db, "ebseq_gene_ln") %>%
select(gene, PostFC) %>%
rename(ln=gene), copy=T) %>%
rename(`L. niger FC` = PostFC) %>%
left_join(tbl(my_db, "bee_names") %>%
rename(am=gene), copy=T))
num.overlap.an <- nrow(an.oggs) # Count the overlaps
test2 <- overlap.hypergeometric.test(num.overlap.an, n.am, n.ln, num.oggs.an, "Apis and L. niger") # Run the hypergeometric test
# flavus and niger
fn.oggs <- make.OGGs(c("lf", "ln"))[[2]] # Get the orthologous gene list
n.lf <- (tbl(my_db, "ebseq_padj_gene_lf") %>%
filter(gene %in% fn.oggs$lf) %>%
summarise(n=n()) %>% as.data.frame())[1,1] # Count the number of diff expressed genes that appear in the OGG list
n.ln <- (tbl(my_db, "ebseq_padj_gene_ln") %>%
filter(gene %in% fn.oggs$ln) %>%
summarise(n=n()) %>% as.data.frame())[1,1]
num.oggs.fn <- nrow(fn.oggs) # Count the orthologous genes
fn.oggs <- suppressMessages(
fn.oggs %>% filter(ln %in% (tbl(my_db, "ebseq_padj_gene_ln") %>% as.data.frame())[,1],
lf %in% (tbl(my_db, "ebseq_padj_gene_lf") %>% as.data.frame())[,1]) %>%
mutate(Species = "L. flavus and L. niger") %>%
left_join(tbl(my_db, "ebseq_gene_lf") %>%
select(gene, PostFC) %>%
rename(lf=gene), copy=T) %>%
rename(`L. flavus FC` = PostFC) %>%
left_join(tbl(my_db, "ebseq_gene_ln") %>%
select(gene, PostFC) %>%
rename(ln=gene), copy=T) %>%
rename(`L. niger FC` = PostFC) %>%
left_join(tbl(my_db, "lf2am"), copy=T) %>%
left_join(tbl(my_db, "bee_names") %>%
rename(am=gene), copy=T))
num.missing <- sum(is.na(fn.oggs$name))
fn.oggs$name[is.na(fn.oggs$name)] <- paste("Unknown gene", 1:num.missing)
num.overlap.fn <- nrow(fn.oggs) # Count the overlaps
test3 <- overlap.hypergeometric.test(num.overlap.fn,
n.lf, n.ln,
num.oggs.fn,
"L. flavus and L. niger") # Run the hypergeometric test
overlaps <- suppressMessages(
data.frame(name = unique(c(af.oggs$name, an.oggs$name, fn.oggs$name)),
stringsAsFactors = F) %>%
left_join(rbind(af.oggs %>% select(name, starts_with("Apis")),
an.oggs %>% select(name, starts_with("Apis")))) %>%
left_join(rbind(af.oggs %>% select(name, ends_with("flavus FC")),
fn.oggs %>% select(name, ends_with("flavus FC")))) %>%
left_join(rbind(an.oggs %>% select(name, ends_with("niger FC")),
fn.oggs %>% select(name, ends_with("niger FC")))) %>% distinct())
overlaps <- rbind(overlaps[overlaps$name == "myosin light chain alkali-like isoform X5", ],
overlaps[overlaps$name != "myosin light chain alkali-like isoform X5", ])
overlaps$Consistent <- "Yes"
overlaps$Consistent[apply(overlaps[,2:4],1,min,na.rm=T)<1 & apply(overlaps[,2:4],1,max,na.rm=T)>1] <- "No"
for(i in 2:4) overlaps[,i] <- format(round(log2(overlaps[,i]), 3), nsmall = 3)
overlaps[overlaps == " NA"] <- " "
rownames(overlaps) <- NULL
overlap.p.values <- rbind(test1, test2, test3)
rownames(overlap.p.values) <- NULL
all.overlaps <- c(af.oggs$am, an.oggs$am, fn.oggs$am[!is.na(fn.oggs$am)]) %>% unique
Table S6: All orthologous genes that were significantly differentially expressed between pheromone treatments in more than one species. The FC columns give the Log\(_2\) fold-change in expression for each species where the focal gene was significantly differentially expressed, where positive numbers mean it was expressed at a higher level in control animals. The last column highlights genes that responded to treatment in a consistent or inconsistent direction across species. B. terrestris is omitted because neither of its differentially expressed genes were significantly affected by treatment in the other three species.
kable.table(overlaps)
| name | Apis FC | L. flavus FC | L. niger FC | Consistent |
|---|---|---|---|---|
| myosin light chain alkali-like isoform X5 | 0.444 | 0.372 | 0.350 | Yes |
| proteasome subunit beta type-5-like | 0.484 | -0.434 | No | |
| probable Bax inhibitor 1 | 0.447 | -0.167 | No | |
| intracellular protein transport protein USO1 isoform X2 | -0.684 | 0.445 | No | |
| muscle M-line assembly protein unc-89 isoform X5 | -0.526 | 0.213 | No | |
| transitional endoplasmic reticulum ATPase TER94 | 0.544 | -0.306 | No | |
| actin related protein 1 | 0.762 | 0.083 | Yes | |
| tubulin alpha-1 chain-like | 0.773 | -0.251 | No | |
| Unknown gene 1 | -0.088 | 0.048 | No | |
| uncharacterized protein LOC100576760 isoform X2 | -0.066 | -0.163 | Yes | |
| myosin regulatory light chain 2 | 0.258 | 0.279 | Yes | |
| NADP-dependent malic enzyme isoform X3 | 0.040 | -0.067 | No | |
| transketolase isoform 1 | -0.248 | -0.342 | Yes | |
| troponin T, skeletal muscle | 0.374 | 0.185 | Yes | |
| uncharacterized protein LOC551958 | 0.511 | -0.108 | No | |
| probable cytochrome P450 304a1 | -0.224 | 0.470 | No | |
| Unknown gene 2 | 0.181 | 0.092 | Yes | |
| WD repeat-containing protein 37-like isoform X4 | 0.083 | 0.407 | Yes | |
| Unknown gene 3 | -0.131 | -0.211 | Yes | |
| uncharacterized protein LOC409805 isoform X3 | 0.444 | 0.415 | Yes | |
| ADP/ATP translocase | 0.054 | 0.154 | Yes | |
| peroxidase isoformX2 | 0.104 | 0.008 | Yes | |
| neurofilament heavy polypeptide-like isoform X2 | 0.377 | 0.069 | Yes | |
| fatty acid synthase-like isoform 1 | -0.926 | -1.015 | Yes | |
| LOW QUALITY PROTEIN: counting factor associated protein D-like | -0.294 | -0.097 | Yes | |
| myophilin-like | 0.226 | 0.216 | Yes | |
| Unknown gene 4 | 0.039 | 0.254 | Yes | |
| hexaprenyldihydroxybenzoate methyltransferase, mitochondrial-like | 7.514 | -0.368 | No | |
| arginine kinase isoform X2 | 0.441 | 0.141 | Yes | |
| heat shock protein cognate 4 | -0.369 | -0.432 | Yes | |
| tropomyosin-1-like | 0.116 | 0.393 | Yes | |
| 6-phosphogluconate dehydrogenase, decarboxylating | -0.445 | -0.603 | Yes | |
| transaldolase | -0.044 | 0.034 | No | |
| superoxide dismutase 1 | -0.175 | -0.324 | Yes | |
| translation elongation factor 2-like isoform 1 | -0.079 | 0.004 | No | |
| very-long-chain enoyl-CoA reductase-like | -0.201 | -0.431 | Yes | |
| Unknown gene 5 | 0.350 | 0.359 | Yes |
Table S7: The overlap between the lists of significantly differently expressed orthologous genes was significantly higher than expected for L. flavus and L. niger, suggesting that queen pheromone has conserved effects on gene expression between these two species (results based on a hypergeometric test). For the other two species pairs, the number of overlapping genes was not higher or lower than expected under the null hypothesis that queen pheromone affects a random set of genes in each species.
pander(overlap.p.values, split.cell = 40, split.table = Inf)
| Species | Test | p |
|---|---|---|
| Apis and L. flavus | Overlap is higher than expected: | 0.1915 |
| Apis and L. niger | Overlap is higher than expected: | 0.2616 |
| L. flavus and L. niger | Overlap is higher than expected: | 0 |
most.pheromone.sensitive.genes <- function(){
ngenes.list <- (1:5)*100 # 100 - 500
dat <- list()
for(i in 1: length(ngenes.list)){
ngenes <- ngenes.list[i]
# Get the top n genes from Apis, as ranked by the absolute value for the log-fold change in response to pheromone
g1 <- tbl(my_db, "ebseq_gene_am") %>% collect() %>%
select(gene, PostFC) %>%
mutate(PostFC = log2(PostFC)) %>% left_join(tbl(my_db, "bee_names"), copy=TRUE, by = "gene") %>%
arrange(-abs(PostFC)) %>% head(ngenes) %>% .$name %>% unique()
# Do the same for genes from non-Apis species, and get the Apis names for the top BLAST hits in the Apis genome
g2 <- tbl(my_db, "ebseq_gene_bt") %>%
select(gene, PostFC) %>%
left_join(tbl(my_db, "bt2am") %>%
rename(gene = bt) %>%
select(-evalue), by = "gene") %>%
collect() %>% mutate(PostFC = log2(PostFC)) %>%
arrange(-abs(PostFC)) %>%
rename(bt = gene, gene = am) %>%
left_join(tbl(my_db, "bee_names"), copy=TRUE, by = "gene") %>%
filter(!is.na(name)) %>% head(ngenes) %>% .$name %>% unique()
g3 <- tbl(my_db, "ebseq_gene_lf") %>%
select(gene, PostFC) %>%
left_join(tbl(my_db, "lf2am") %>%
rename(gene = lf) %>%
select(-evalue), by = "gene") %>%
collect() %>% mutate(PostFC = log2(PostFC)) %>%
arrange(-abs(PostFC)) %>%
rename(lf = gene, gene = am) %>%
left_join(tbl(my_db, "bee_names"), copy=TRUE, by = "gene") %>%
filter(!is.na(name)) %>% head(ngenes) %>% .$name %>% unique()
g4 <-tbl(my_db, "ebseq_gene_ln") %>%
select(gene, PostFC) %>%
left_join(tbl(my_db, "ln2am") %>%
rename(gene = ln) %>%
select(-evalue), by = "gene") %>%
collect() %>% mutate(PostFC = log2(PostFC)) %>%
arrange(-abs(PostFC)) %>%
rename(ln = gene, gene = am) %>%
left_join(tbl(my_db, "bee_names"), copy=TRUE, by = "gene") %>%
filter(!is.na(name)) %>% head(ngenes) %>% .$name %>% unique()
# Count the number of intersections, and find gene names that appear in 3 or 4 species using the venn() function
venn.diagram <- venn(list(am=g1, bt=g2, lf=g3, ln=g4), show.plot=FALSE)
three.plus <- attr(venn.diagram, "intersections")[str_count(names(attr(venn.diagram, "intersections")), ":") > 1] %>%
unlist %>% unname %>% unique %>% sort
four <- attr(venn.diagram, "intersections")[str_count(names(attr(venn.diagram, "intersections")), ":") > 2] %>%
unlist %>% unname %>% unique %>% sort
three <- three.plus[!(three.plus %in% four)]
if(length(three) + length(four) > 0) dat[[i]] <- data.frame(Name = c(three, four),
count = c(rep("x3 species", length(three)),
rep("4 species", length(four))),
nGenes = ngenes, stringsAsFactors = FALSE)
}
dat <- do.call("rbind", dat) %>%
arrange(count, nGenes, Name) %>%
distinct(paste(Name, count), .keep_all = TRUE) %>%
select(Name, count, nGenes) %>%
mutate(count = replace(count, count == "x3 species", "3 species"))
names(dat) <- c("Name", "Appears in", "Size of gene set")
dat
}
most.pheromone.sensitive.genes <- most.pheromone.sensitive.genes()
Table S8: List of genes that appear in the top n-most pheromone-sensitive genes for 3 or 4 species. To generate the table, we ranked genes by the absolute value of their log fold change in response to queen pheromone, then listed the gene names that appeared in 3-4 species. For non-Apis species, we found the gene names by comparison with the Apis genome by BLAST. This exercise was performed with n = 100, 200 … 500, and the third column lists the smallest n for which the gene in question appeared (for example, the gene protein takeout-like appeared for all 4 species when inspecting the top 200+ genes).
kable(most.pheromone.sensitive.genes, "html") %>%
kable_styling() %>%
scroll_box(height = "300px")
| Name | Appears in | Size of gene set |
|---|---|---|
| protein takeout-like | 4 species | 200 |
| glucose dehydrogenase [FAD, quinone] | 4 species | 300 |
| histone-lysine N-methyltransferase SETMAR-like | 4 species | 300 |
| serotonin receptor | 4 species | 500 |
| titin-like | 4 species | 500 |
| uncharacterized protein LOC102656088 | 4 species | 500 |
| histone-lysine N-methyltransferase SETMAR-like | 3 species | 200 |
| 2-oxoglutarate dehydrogenase, mitochondrial-like isoform X5 | 3 species | 300 |
| probable serine/threonine-protein kinase DDB_G0282963 isoform X4 | 3 species | 300 |
| titin-like | 3 species | 300 |
| elongation of very long chain fatty acids protein 6-like | 3 species | 400 |
| ligand-gated chloride channel homolog 3 precursor | 3 species | 400 |
| odorant receptor Or2-like | 3 species | 400 |
| putative odorant receptor 13a-like | 3 species | 400 |
| serotonin receptor | 3 species | 400 |
| trypsin-1 | 3 species | 400 |
| uncharacterized protein LOC100576902 | 3 species | 400 |
| uncharacterized protein LOC102655422 | 3 species | 400 |
| uncharacterized protein LOC102656088 | 3 species | 400 |
| metabotropic glutamate receptor 7 isoform X3 | 3 species | 500 |
| probable cytochrome P450 305a1 | 3 species | 500 |
| protein NPC2 homolog | 3 species | 500 |
| suppressor protein SRP40-like | 3 species | 500 |
| uncharacterized protein LOC100577132 | 3 species | 500 |
| uncharacterized protein LOC102656830 | 3 species | 500 |
| uncharacterized protein LOC724216 | 3 species | 500 |
We defined a gene as “evolutionarily ancient” if it has an ortholog in at least one species from the other lineage (for example, we define ancient A. mellifera genes as those that have a reciprocal best BLAST hit in one or both Lasius species). Genes that were not detected by BLAST in the other lineage were defined as putatively lineage-specific (though many of them are likely to be conserved genes that we failed to identify as such, hence the word “putative”). Using a Chi-square test, we find that genes that are significantly differentially expressed in response to queen pheromone are more likely to be ancient than those that are not differentially exressed. This relationship holds for all three species for which we found differential expression, and for genes that were higher or lower in the pheromone treatment. The fact that we probably miscalssifed many genes as ancient vs lineage-specific means that the result is likely to be even stronger than suggested here.
ancient.genes.test <- function(species){
if(species == "am") ancient.genes <- c(make.OGGs(c("am", "lf"))[[2]]$am,
make.OGGs(c("am", "ln"))[[2]]$am) %>% unique
if(species == "bt") ancient.genes <- c(make.OGGs(c("bt", "lf"))[[2]]$bt,
make.OGGs(c("bt", "ln"))[[2]]$bt) %>% unique
if(species == "lf") ancient.genes <- c(make.OGGs(c("lf", "am"))[[2]]$lf,
make.OGGs(c("lf", "bt"))[[2]]$lf) %>% unique
if(species == "ln") ancient.genes <- c(make.OGGs(c("ln", "am"))[[2]]$ln,
make.OGGs(c("ln", "bt"))[[2]]$am) %>% unique
lab <- "Putatively bee-specific"
if(species %in% c("lf", "ln")) lab <- "Putatively ant-specific"
expression <- tbl(my_db, paste("ebseq_gene_", species, sep="")) %>%
select(gene, PostFC) %>% collect() %>%
mutate(age = lab, sig = "Non-sig") %>% as.data.frame()
expression$age[expression$gene %in% ancient.genes] <- "Evolutionarily ancient"
expression$sig[expression$gene %in% (tbl(my_db, paste("ebseq_padj_gene_", species, sep="")) %>%
filter(PostFC < 1) %>% select(gene) %>% collect %>% .$gene)] <- "Up in QP"
expression$sig[expression$gene %in% (tbl(my_db, paste("ebseq_padj_gene_", species, sep="")) %>%
filter(PostFC > 1) %>% select(gene) %>% collect %>% .$gene)] <- "Up in Control"
tab <- table(expression$sig, expression$age)
chisq.test(tab) %>% print
percent <- paste("(", (100*tab / rowSums(tab)) %>% round(1) %>% format(nsmall=1), "%)", sep = "")
for(i in 1:2) {for(j in 1:3) tab[j,i] <- paste(tab[j,i], percent[j + (i-1)*3])}
tab %>% pander
}
ancient.genes.test("am")
##
## Pearson's Chi-squared test
##
## data: tab
## X-squared = 43.581, df = 2, p-value = 3.439e-10
| Evolutionarily ancient | Putatively bee-specific | |
|---|---|---|
| Non-sig | 5461 (47.4%) | 6061 (52.6%) |
| Up in Control | 150 (70.1%) | 64 (29.9%) |
| Up in QP | 54 (50.0%) | 54 (50.0%) |
ancient.genes.test("lf")
##
## Pearson's Chi-squared test
##
## data: tab
## X-squared = 344.8, df = 2, p-value < 2.2e-16
| Evolutionarily ancient | Putatively ant-specific | |
|---|---|---|
| Non-sig | 7167 (14.4%) | 42488 (85.6%) |
| Up in Control | 76 (41.5%) | 107 (58.5%) |
| Up in QP | 72 (67.3%) | 35 (32.7%) |
ancient.genes.test("ln")
##
## Pearson's Chi-squared test
##
## data: tab
## X-squared = 16.823, df = 2, p-value = 0.0002223
| Evolutionarily ancient | Putatively ant-specific | |
|---|---|---|
| Non-sig | 4524 (23.0%) | 15129 (77.0%) |
| Up in Control | 30 (42.9%) | 40 (57.1%) |
| Up in QP | 19 (29.2%) | 46 (70.8%) |
These tests ask if genes that are up-regulated in the queen pheromone treatment in one species are also up (or down) regulated in another. These tests used fold expression changes calculated using ebseq, after omitting the four irregular Lasius samples. The advantage of these tests is that one is not limited to the set of ‘significant’ genes, which discards a lot of information based on an arbitrary p-value threshold.
get.fc.for.pair.species <- function(species1, species2){
query <- 'SELECT rbb.X AS X_gene, rbb.Y AS Y_gene, ebseq_gene_X.PostFC AS X_fc, ebseq_gene_Y.PostFC AS Y_fc FROM ebseq_gene_X
JOIN
(SELECT Y2X.X, Y2X.Y FROM Y2X
JOIN X2Y
ON Y2X.Y = X2Y.Y AND Y2X.X = X2Y.X ) AS rbb
ON rbb.X = ebseq_gene_X.gene
JOIN ebseq_gene_Y
ON rbb.Y = ebseq_gene_Y.gene'
query <- str_replace_all(query, "X", species1)
query <- str_replace_all(query, "Y", species2)
dbGetQuery(db, query)
}
Table S9: Results of Spearman’s rank correlations, testing whether the absolute log fold difference between pheromones treatments is correlated for a given pair of species. Positive coefficients (rho) indicate that on average, orthologous genes have similar sensitivity to queen pheromones. The p-values have been corrected for multiple testing with the Benjamini-Hochberg method.
species.combinations <- t(combn(c("am", "bt", "lf", "ln"), 2))
rho <- numeric(nrow(species.combinations))
p <- numeric(nrow(species.combinations))
for(i in 1:nrow(species.combinations)){
fc.data <- get.fc.for.pair.species(species.combinations[i, 1],
species.combinations[i,2])
fc.data[,3:4] <- fc.data[,3:4] %>% log2 %>% abs # Log the fold changes - not that it matters for Spearman's!
results <- suppressWarnings(with(fc.data, cor.test(fc.data[,3],
fc.data[,4], method="spearman"))) # Spearman's correlation
rho[i] <- results$estimate
p[i] <- results$p.value
}
species.combinations <- data.frame(Species1 = species.combinations[,1],
Species2 = species.combinations[,2],
rho = rho,
p = p.adjust(p, method = "BH"), # adjust these p-vals for multiple testing
sig = " ", stringsAsFactors = F)
species.combinations[species.combinations == "am"] <- "Apis mellifera"
species.combinations[species.combinations == "bt"] <- "Bombus terrestris"
species.combinations[species.combinations == "lf"] <- "Lasius flavus"
species.combinations[species.combinations == "ln"] <- "Lasius niger"
species.combinations$sig[species.combinations$p < 0.05] <- "*"
species.combinations$sig[species.combinations$p < 0.01] <- "**"
species.combinations$sig[species.combinations$p < 0.0001] <- "***"
# Make a table
species.combinations %>% mutate(rho = format(round(rho, 3), nsmall = 3)) %>% pander
| Species1 | Species2 | rho | p | sig |
|---|---|---|---|---|
| Apis mellifera | Bombus terrestris | 0.136 | 3.232e-24 | *** |
| Apis mellifera | Lasius flavus | 0.100 | 1.478e-12 | *** |
| Apis mellifera | Lasius niger | 0.077 | 1.853e-07 | *** |
| Bombus terrestris | Lasius flavus | 0.159 | 3.112e-39 | *** |
| Bombus terrestris | Lasius niger | 0.127 | 2.282e-24 | *** |
| Lasius flavus | Lasius niger | 0.194 | 3.765e-61 | *** |
# Make a figure
heat.map.figure <- species.combinations %>% ggplot(aes(Species1, Species2, fill=rho)) +
geom_tile(colour="white", size=4) +
scale_fill_gradient2(name = "Corr",
low = brewer.pal(9, "RdYlBu")[7],
mid = "white",
high = brewer.pal(9, "RdYlBu")[2]) +
geom_text(aes(label = paste(format(signif(rho, 2), nsmall = 2), sig)), size = 3.5) +
theme_bw() + theme(panel.grid = element_blank(),
panel.border = element_blank(),
axis.ticks = element_blank(),
axis.text = element_text(face = "italic"),
legend.position = "none") +
xlab(NULL) + ylab(NULL) +
scale_x_discrete(labels = c("Apis\nmellifera", "Bombus\nterrestris", "Lasius\nflavus"), expand = c(0,0)) +
scale_y_discrete(labels = c("Bombus\nterrestris", "Lasius\nflavus", "Lasius\nniger"), expand = c(0,0))
heat.map.figure
ggsave(heat.map.figure, file = "figures/Correlations heat map.pdf", height = 4, width=4.3)
Figure S3: Results of Spearman’s rank correlations, testing whether the fold-change in gene expression in response to queen pheromone is correlated for a given pair of species. The colour shows the correlation (Spearman’s rho), where red indicates that on average, orthologous genes are affected in the same direction by queen pheromones, and blue indicates the reverse. The stars show the degree of statistical significance after FDR correction (** p < 0.01, *** p < 0.0001).
Many genes showed alternative splicing in all four species, with the great majority showing between 1 and 6 isoforms.
rbind(my_db %>% tbl("isoforms_am") %>% collect %>% .$gene %>%
table %>% melt %>% select(value) %>% mutate(sp = "Apis mellifera"),
my_db %>% tbl("isoforms_bt") %>% collect %>% .$gene %>%
table %>% melt %>% select(value) %>% mutate(sp = "Bombus terrestris"),
my_db %>% tbl("isoforms_lf") %>% collect %>% .$gene %>%
table %>% melt %>% select(value) %>% mutate(sp = "Lasius niger"),
my_db %>% tbl("isoforms_ln") %>% collect %>% .$gene %>%
table %>% melt %>% select(value) %>% mutate(sp = "Lasius flavus")) %>%
as.data.frame() %>%
ggplot(aes(x = value, y = sp, fill = sp)) +
geom_joy(stat = "binline", binwidth=1) +
coord_cartesian(xlim=c(1,12)) +
scale_fill_cyclical(values = c("#4040B0", "#9090F0")) +
scale_x_continuous(breaks = seq(1,12,by=1)) +
scale_y_discrete(expand = c(0.01, 0)) +
theme_joy() +
xlab("Number of isoforms") + ylab(NULL) +
theme(axis.text = element_text(face = "italic"))
Figure S4: Distribution of isoform numbers per gene for each of the four species.
# Define a function to search for significantly alternatively spliced genes. We define these as genes that have at least two differentially expressed isoforms, where queen pheromone stimulates expresison of one isoform but surpresses expression of another
find.alternatively.spliced.genes <- function(species){
# Write a database query with 'X' as a placeholder for the species name
# We want to find genes in which at least two isoforms are differentially expressed in response to pheromones
# Significant isoforms are listed in the ebseq_padj_isoform_X tables, so we count them and get the names of their genes
query <- 'SELECT isoforms_X.gene, isoforms_X.isoform, PostFC FROM isoforms_X
JOIN
(SELECT gene, COUNT(*) FROM ebseq_padj_isoform_X
JOIN isoforms_X
ON isoforms_X.isoform = ebseq_padj_isoform_X.isoform
GROUP BY gene
HAVING COUNT(*)>1 ) AS multiISO
ON multiIso.gene = isoforms_X.gene
JOIN ebseq_padj_isoform_X
ON ebseq_padj_isoform_X.isoform = isoforms_X.isoform
ORDER BY isoforms_X.gene'
query <- str_replace_all(query, "X", species) # replace X with the species
Splice <- dbGetQuery(db, query) # run the query
# Find the highest and lowest fold change for the isoforms of each gene
SpliceMin <- aggregate(Splice$PostFC, by=list(Splice$gene), FUN="min")
SpliceMax <- aggregate(Splice$PostFC, by=list(Splice$gene), FUN="max")
SpliceCompare <- merge(SpliceMin, SpliceMax, by = "Group.1")
colnames(SpliceCompare) <- c("gene", "min", "max")
# Define diff-spliced genes as those with both elevated and
# repressed isoforms, when comparing control and pheromone-treated workers
output <- data.frame(gene = SpliceCompare$gene[SpliceCompare$min < 1 & SpliceCompare$max > 1], stringsAsFactors = F)
# Add the Apis mellifera ortholog, from one-way BLAST, if it's a non-Apis species
if(species != "am"){
orthologs <- tbl(my_db, paste(species, "2am", sep = "")) %>% select(-evalue) %>% collect(n=Inf) %>% as.data.frame()
names(orthologs) <- c("gene", "Amel_ortholog")
output <- left_join(output, orthologs, by = "gene")
output <- left_join(output, tbl(my_db, "bee_names") %>%
rename(Amel_ortholog = gene), copy=T, by = "Amel_ortholog")
}
else output <- left_join(output, tbl(my_db, "bee_names"), by = "gene", copy = T)
output[is.na(output)] <- " "
# Remove the 'isoform X' part from the gene name, so it gives the name of the gene not the isoform
output$name <- unlist(lapply(strsplit(output$name, split = " isoform "), function(x) x[1]))
output <- left_join(output, SpliceCompare, by = "gene")
output$min <- log2(output$min) # Log2 transform the fold changes
output$max <- log2(output$max)
output <- output %>% arrange(-(abs(min) + max)) # Arrange by effect size
if(species == "am" | species == "bt") names(output) <- c("Gene", "Name", "Lowest FC", "Highest FC")
else names(output) <- c("Gene", "Amel ortholog", "Name", "Lowest FC", "Highest FC")
output
}
Table S10: List of genes showing statistically significant pheromone-induced alternative splicing in A. mellifera. These genes were defined as those that have at least two isoforms that are differentially expressed following pheromone treatment with p < 10-5, and for which one isoform increases in expression while another decreases. The last two columns show the fold changes of the most down-regulated and most up-regulated isoforms, on a Log\(_2\) scale.
am.alt.splice <- find.alternatively.spliced.genes("am")
kable.table(am.alt.splice)
| Gene | Name | Lowest FC | Highest FC |
|---|---|---|---|
| GB44254 | uncharacterized protein LOC411586 | -10.2106382 | 7.3294705 |
| GB55598 | troponin I | -8.6184698 | 7.4257311 |
| GB55650 | ryanodine receptor 44F | -8.6521541 | 6.1211069 |
| GB42000 | cAMP-specific 3’,5’-cyclic phosphodiesterase, isoforms N/G | -7.8461925 | 6.4652082 |
| GB49567 | sestrin-1-like isoformX1 | -6.7384430 | 6.3303655 |
| GB46113 | uncharacterized protein LOC726188 | -6.7215768 | 6.2049532 |
| GB55237 | disco-interacting protein 2 | -6.4126080 | 5.7870758 |
| GB44556 | uncharacterized protein LOC411962 | -5.3193508 | 6.4264182 |
| GB50923 | serine-protein kinase ATM | -5.4981139 | 6.1549064 |
| GB50941 | phosphatidate phosphatase LPIN2-like | -6.1378916 | 5.3694436 |
| GB55848 | DNA ligase 1-like | -6.0254223 | 5.3645877 |
| GB42142 | nuclear hormone receptor FTZ-F1 | -6.0475859 | 5.2543590 |
| GB45259 | zinc finger protein 91-like | -5.7141149 | 5.4922565 |
| GB52595 | zinc finger and BTB domain-containing protein 20-like | -6.0058327 | 5.1479879 |
| GB55225 | sushi, von Willebrand factor type A, EGF and pentraxin domain-containing protein 1 | -3.5827048 | 7.3608415 |
| GB55102 | F-box only protein 28-like | -5.6780118 | 5.1328776 |
| GB42895 | trichohyalin-like | -6.0749616 | 4.6900449 |
| GB44373 | protein zyg-11 homolog B-like | -2.7153166 | 7.8600431 |
| GB49111 | neuropathy target esterase sws | -1.8617078 | 8.3596119 |
| GB46271 | protein BCL9 homolog | -3.1471390 | 6.9356291 |
| GB53431 | inositol hexakisphosphate kinase 2-like | -6.3417004 | 3.3365701 |
| GB44336 | protein couch potato-like | -2.1830854 | 7.3541749 |
| GB45277 | multidrug resistance-associated protein 4-like | -8.1135336 | 1.3365168 |
| GB40263 | dentin sialophosphoprotein-like | -3.0597817 | 6.2723878 |
| 725417 | uncharacterized protein LOC725417 | -2.8308639 | 6.1603441 |
| GB55517 | uncharacterized protein LOC410000 | -3.2763532 | 5.3768010 |
| GB55429 | CREB-regulated transcription coactivator 1-like | -5.3728279 | 3.1844409 |
| GB55998 | beta-1,4-N-acetylgalactosaminyltransferase bre-4 | -2.7284140 | 5.5956924 |
| GB52604 | LIM domain-binding protein 2-like | -2.2872276 | 5.8679044 |
| GB41734 | reversion-inducing-cysteine-rich protein with kazal motifs | -5.9697261 | 1.9393374 |
| GB49535 | calcium/calmodulin-dependent protein kinase II | -1.9949124 | 5.8059893 |
| GB45662 | conserved oligomeric Golgi complex subunit 4-like | -5.3583810 | 2.1410794 |
| GB40310 | uncharacterized protein LOC411575 | -0.9447237 | 6.4575407 |
| GB51117 | rho GTPase-activating protein 18-like | -0.9711563 | 6.3563951 |
| GB41129 | protein LMBR1L-like | -5.6199019 | 1.4425609 |
| GB44876 | uncharacterized protein LOC100576421 | -5.3652303 | 1.6410521 |
| GB50244 | NHL repeat-containing protein 2 | -0.9371409 | 5.9580141 |
| GB47138 | calcium-activated potassium channel slowpoke-like | -0.9035332 | 5.9504672 |
| GB50099 | uncharacterized abhydrolase domain-containing protein DDB_G0269086-like | -1.5085077 | 5.0811380 |
| GB41908 | PERQ amino acid-rich with GYF domain-containing protein CG11148-like | -1.0050181 | 5.5164280 |
| GB52999 | neurofilament heavy polypeptide-like | -2.7388052 | 3.6790149 |
| GB51651 | putative inorganic phosphate cotransporter-like | -5.4170376 | 0.9305746 |
| GB50877 | tyrosine-protein kinase Dnt | -2.5061716 | 3.1568560 |
| GB43220 | transcription termination factor 2 | -3.2229375 | 1.8337147 |
| GB40565 | ribosomal protein S6 kinase alpha-5 | -2.3132702 | 2.6623092 |
| GB55467 | neural cell adhesion molecule L1-like | -3.3341247 | 1.4565432 |
| GB48034 | protein numb-like, transcript variant X5 | -1.0127583 | 3.7699557 |
| GB55570 | transmembrane protein 53-like | -2.0692979 | 2.6556081 |
| GB49417 | PITH domain-containing protein GA19395-like | -2.1836294 | 2.2457448 |
| GB43282 | guanine nucleotide-binding protein G(q) subunit alpha-like | -2.3600303 | 2.0113196 |
| GB48573 | probable multidrug resistance-associated protein lethal(2)03659-like | -2.1285308 | 1.9867141 |
| GB50366 | uncharacterized protein LOC551450 | -0.8408050 | 1.1435481 |
| GB46121 | ubiquitin fusion degradation protein 1 homolog | -0.9511837 | 0.9182434 |
| GB52052 | venom carboxylesterase-6-like | -0.7021931 | 0.9102424 |
Table S11: List of genes showing statistically significant pheromone-induced alternative splicing in L. flavus. The table shows the same information as Table S10.
lf.alt.splice<- find.alternatively.spliced.genes("lf")
kable.table(lf.alt.splice)
| Gene | Amel ortholog | Name | Lowest FC | Highest FC |
|---|---|---|---|---|
| TRINITY_DN11346_c0_g1 | GB49250 | heme oxygenase | -9.1733822 | 4.2807355 |
| TRINITY_DN14030_c0_g1 | XP_016769715.1 | -4.5698062 | 6.1058670 | |
| TRINITY_DN13728_c1_g1 | GB44606 | AMP deaminase 2-like | -5.6147192 | 4.2278104 |
| TRINITY_DN13759_c0_g1 | XP_016766389.1 | -3.7805082 | 5.5650278 | |
| TRINITY_DN13897_c0_g1 | GB41293 | histone acetyltransferase KAT8 | -4.6420034 | 2.6858828 |
| TRINITY_DN14126_c1_g2 | GB43039 | restin homolog | -1.8789713 | 5.3598354 |
| TRINITY_DN12581_c0_g2 | XP_016767063.1 | -4.1075789 | 2.7973408 | |
| TRINITY_DN14084_c0_g1 | XP_016772396.1 | -2.4056262 | 4.1607373 | |
| TRINITY_DN13929_c0_g1 | GB53852 | paired amphipathic helix protein Sin3a | -2.0878837 | 4.4200505 |
| TRINITY_DN13956_c0_g1 | GB54341 | RNA-binding protein 33-like | -1.9836823 | 4.5150571 |
| TRINITY_DN13699_c0_g1 | GB41835 | sorting nexin-13-like | -2.5195188 | 3.9141700 |
| TRINITY_DN13676_c0_g1 | XP_016767354.1 | -3.9853775 | 2.2791646 | |
| TRINITY_DN13889_c0_g1 | GB44338 | small G protein signaling modulator 3 homolog | -2.6671307 | 3.5553713 |
| TRINITY_DN11861_c1_g1 | GB43504 | neural/ectodermal development factor IMP-L2 | -2.2204311 | 3.4241368 |
| TRINITY_DN14001_c0_g2 | GB41033 | facilitated trehalose transporter Tret1-like | -3.4253663 | 2.1957523 |
| TRINITY_DN12063_c0_g1 | GB49936 | calcium uptake protein 1 homolog, mitochondrial-like | -1.9568877 | 3.6347798 |
| TRINITY_DN13321_c0_g1 | XP_016769905.1 | -2.8397819 | 2.7402835 | |
| TRINITY_DN13931_c4_g1 | GB47270 | cytochrome P450 4C1 | -2.2502914 | 2.8866039 |
| TRINITY_DN12721_c1_g1 | GB43391 | transmembrane protein 8B-like | -2.1793408 | 2.8228945 |
| TRINITY_DN11401_c0_g1 | GB50510 | uncharacterized protein LOC409674 | -2.6928098 | 1.9864175 |
| TRINITY_DN10695_c0_g1 | XP_016773356.1 | -2.1193002 | 2.4882173 | |
| TRINITY_DN13698_c3_g1 | GB45025 | mTERF domain-containing protein 1, mitochondrial-like | -1.9661074 | 2.5552928 |
| TRINITY_DN13919_c0_g1 | GB49593 | cytosolic carboxypeptidase-like protein 5-like | -1.6893918 | 2.7745341 |
| TRINITY_DN14156_c10_g1 | XP_016768402.1 | -2.0840677 | 2.3753245 | |
| TRINITY_DN13974_c0_g1 | XP_016768210.1 | -1.5945919 | 2.7670315 | |
| TRINITY_DN12596_c0_g1 | GB40801 | thioredoxin-like protein 4A-like | -1.7080464 | 2.3372385 |
| TRINITY_DN13248_c0_g1 | GB42981 | beta-1,3-glucan-binding protein | -1.6951844 | 2.3160927 |
| TRINITY_DN14247_c8_g2 | GB52590 | fatty acid synthase-like | -1.0570339 | 1.0113553 |
| TRINITY_DN10832_c0_g1 | GB54056 | serine hydroxymethyltransferase, cytosolic | -1.2534345 | 0.3609471 |
| TRINITY_DN11786_c1_g1 | GB51214 | troponin T, skeletal muscle | -0.4087698 | 0.8466319 |
| TRINITY_DN13339_c0_g1 | GB40735 | fructose-bisphosphate aldolase-like | -0.1714515 | 0.3993615 |
| TRINITY_DN13721_c8_g1 | XP_016772716.1 | -0.2069941 | 0.2124566 | |
| TRINITY_DN13271_c0_g1 | GB40312 | choline/ethanolamine kinase-like | -0.1549773 | 0.0102486 |
| TRINITY_DN10322_c0_g1 | XP_016769014.1 | -0.1131430 | 0.0289235 |
Table S12: List of genes showing statistically significant pheromone-induced alternative splicing in L. niger. The table shows the same information as Table S10.
ln.alt.splice <- find.alternatively.spliced.genes("ln")
kable.table(ln.alt.splice)
| Gene | Amel ortholog | Name | Lowest FC | Highest FC |
|---|---|---|---|---|
| RF55_752 | GB48208 | protein argonaute-2 | -3.2926101 | 6.4472781 |
| RF55_883 | XP_016770988.1 | -5.9073798 | 3.5987463 | |
| RF55_4195 | XP_016772612.1 | -5.1744722 | 4.3092261 | |
| RF55_412 | XP_016770021.1 | -3.3875926 | 5.9670345 | |
| RF55_2523 | XP_016770619.1 | -4.7649090 | 4.0350580 | |
| RF55_3907 | XP_016771611.1 | -4.4508904 | 3.6861314 | |
| RF55_4516 | GB54906 | niemann-Pick C1 protein-like | -3.7980002 | 4.3024830 |
| RF55_2336 | GB54910 | tyrosine-protein kinase Abl-like | -3.2249951 | 4.4534584 |
| RF55_1192 | XP_016769850.1 | -1.9480198 | 5.7297004 | |
| XLOC_016164 | -5.4972688 | 2.1282740 | ||
| RF55_3254 | XP_016773300.1 | -2.7312184 | 4.8910736 | |
| RF55_1559 | XP_016768510.1 | -2.9908389 | 4.3225630 | |
| RF55_4335 | XP_016767803.1 | -3.8099604 | 3.4311823 | |
| RF55_6516 | GB40718 | thioredoxin reductase 1 | -3.2537489 | 3.9222290 |
| RF55_11163 | GB53163 | transient receptor potential channel pyrexia | -3.9015904 | 3.2568624 |
| RF55_1926 | XP_016766364.1 | -1.7898846 | 5.3146852 | |
| RF55_9605 | GB42484 | aminopeptidase N-like isoformX1 | -5.0263823 | 2.0370079 |
| XLOC_003165 | -0.6701274 | 6.3901363 | ||
| RF55_4472 | GB43953 | cycle | -3.9049333 | 3.0344073 |
| RF55_13096 | XP_016767210.1 | -4.8346835 | 2.0905931 | |
| RF55_9014 | GB55507 | FYVE, RhoGEF and PH domain-containing protein 4-like | -3.9205477 | 2.9639182 |
| RF55_8972 | XP_016771571.1 | -4.8894254 | 1.9830903 | |
| RF55_4341 | XP_392463.4 | -3.2324663 | 3.6096634 | |
| XLOC_013280 | -2.4206648 | 4.3918399 | ||
| RF55_2163 | GB55475 | cullin-5 | -1.9499220 | 4.8473456 |
| RF55_1574 | XP_016770060.1 | -0.5327703 | 6.2375585 | |
| RF55_6406 | XP_016767146.1 | -2.0553009 | 4.6650121 | |
| RF55_1819 | GB51068 | arrestin homolog | -2.3004627 | 4.3994752 |
| RF55_2357 | XP_016769793.1 | -4.9713497 | 1.7125669 | |
| RF55_2452 | XP_016767413.1 | -4.9414495 | 1.6803943 | |
| RF55_764 | XP_001121384.4 | -4.4683077 | 2.1308271 | |
| RF55_5343 | XP_016766531.1 | -3.3768061 | 3.2009350 | |
| RF55_2401 | XP_016769193.1 | -3.8965864 | 2.6724345 | |
| RF55_6625 | XP_016770656.1 | -2.0711259 | 4.4766181 | |
| RF55_4021 | XP_016767419.1 | -1.8167853 | 4.6555595 | |
| RF55_317 | XP_016769975.1 | -2.7140799 | 3.7123571 | |
| RF55_561 | GB51542 | PH-interacting protein | -3.3596059 | 2.9952497 |
| RF55_2755 | GB48836 | uncharacterized protein LOC100577578 | -4.5392256 | 1.7981131 |
| RF55_357 | -4.0137355 | 2.2850079 | ||
| RF55_9274 | XP_016767607.1 | -4.1097469 | 2.1003576 | |
| RF55_1902 | GB46211 | zinc finger protein 665-like | -4.2211377 | 1.9522150 |
| RF55_1336 | XP_016767701.1 | -4.2155289 | 1.9317851 | |
| RF55_1520 | XP_016768717.1 | -2.0486448 | 4.0217111 | |
| RF55_2217 | GB47260 | zinc finger protein 598-like | -1.9608779 | 4.1054197 |
| RF55_6360 | XP_003251881.3 | -3.5776193 | 2.4733234 | |
| RF55_15946 | XP_016767569.1 | -2.3204379 | 3.7235457 | |
| RF55_4138 | XP_016766515.1 | -2.3589464 | 3.6642057 | |
| RF55_1328 | GB41746 | neogenin | -2.0301217 | 3.8766286 |
| RF55_6748 | GB52716 | NAD kinase-like, transcript variant X11 | -3.4936440 | 2.3932969 |
| RF55_7315 | GB55434 | rab GDP dissociation inhibitor beta | -3.1288936 | 2.7150106 |
| RF55_9900 | XP_016767864.1 | -3.5513206 | 2.2796009 | |
| RF55_1325 | GB44695 | lysophospholipase-like protein 1-like | -4.0976819 | 1.6743676 |
| RF55_9036 | XP_016768958.1 | -3.9412444 | 1.7818052 | |
| RF55_742 | XP_016769412.1 | -2.7605014 | 2.9581890 | |
| RF55_9907 | GB47039 | dynamin | -3.9896574 | 1.7131009 |
| RF55_9185 | XP_016768847.1 | -3.8364223 | 1.8598316 | |
| RF55_2976 | GB42054 | sodium/potassium-transporting ATPase subunit alpha | -2.0568520 | 3.6039514 |
| RF55_4649 | GB43618 | aconitate hydratase, mitochondrial-like | -5.0413696 | 0.5716779 |
| RF55_12355 | GB42664 | probable ATP-dependent RNA helicase DDX43-like | -1.9943294 | 3.6184641 |
| RF55_1934 | GB54827 | synaptotagmin 1 | -5.3908347 | 0.1905938 |
| RF55_360 | GB46768 | uncharacterized MFS-type transporter C09D4.1-like | -3.2312572 | 2.3204411 |
| RF55_5123 | XP_016772933.1 | -2.7363919 | 2.8109308 | |
| RF55_3009 | GB53317 | dentin sialophosphoprotein-like | -3.7638023 | 1.7787767 |
| RF55_5073 | GB55540 | zinc finger MYM-type protein 3-like | -1.8616556 | 3.6633963 |
| RF55_9319 | XP_016768793.1 | -1.6023217 | 3.8961635 | |
| RF55_952 | GB42014 | E3 ubiquitin-protein ligase TRIP12-like | -1.6637152 | 3.6314244 |
| RF55_3561 | GB41659 | endothelin-converting enzyme 1 | -1.9116224 | 3.3339080 |
| RF55_4175 | GB44311 | actin related protein 1 | -1.4407595 | 3.7728266 |
| RF55_7804 | -2.5441138 | 2.6300085 | ||
| RF55_1689 | XP_016768411.1 | -3.3768014 | 1.7465719 | |
| RF55_5052 | XP_016773337.1 | -2.4182694 | 2.6840874 | |
| RF55_457 | GB40931 | uncharacterized protein LOC409781 | -2.3507186 | 2.6953986 |
| RF55_7632 | XP_016767095.1 | -2.0462508 | 2.9941556 | |
| RF55_11518 | GB41804 | nardilysin | -2.2810020 | 2.7512083 |
| RF55_4355 | XP_016771542.1 | -2.4450723 | 2.5183903 | |
| RF55_1518 | XP_016768753.1 | -3.0929627 | 1.8614463 | |
| RF55_5804 | XP_016766957.1 | -2.6227377 | 2.2732244 | |
| RF55_4425 | GB51264 | glutamine-dependent NAD(+) synthetase, transcript variant X3 | -2.1938416 | 2.6792288 |
| RF55_5947 | XP_016768497.1 | -2.0359071 | 2.6987690 | |
| RF55_3209 | GB46684 | monocarboxylate transporter 3-like | -2.2501560 | 2.4459333 |
| RF55_4132 | XP_006572145.2 | -1.8924997 | 2.7949094 | |
| RF55_3822 | XP_016769466.1 | -2.5889623 | 2.0767884 | |
| RF55_8207 | XP_016767693.1 | -2.6776356 | 1.9612772 | |
| RF55_3129 | GB53974 | probable RNA helicase armi | -2.4754839 | 2.1042263 |
| RF55_8822 | GB41970 | ras-like protein 2-like | -2.5012521 | 2.0767873 |
| RF55_9449 | GB55840 | protein sidekick-1-like | -1.9739288 | 2.4747175 |
| RF55_583 | GB41366 | protein MLP1-like | -2.5149738 | 1.9248983 |
| RF55_5597 | GB46705 | muscle M-line assembly protein unc-89 | -4.2010432 | 0.1942554 |
| RF55_7779 | GB40928 | tripartite motif-containing protein 2-like | -1.9058556 | 2.4627030 |
| RF55_1209 | XP_016766933.1 | -1.8405716 | 2.4685968 | |
| RF55_2958 | XP_016771468.1 | -2.2465795 | 1.9449655 | |
| RF55_7227 | GB45211 | troponin C type I | -3.4951202 | 0.6960651 |
| RF55_15397 | XP_016766611.1 | -2.1887540 | 1.9674339 | |
| RF55_3792 | GB42024 | translation initiation factor 2 | -2.3474211 | 1.7699710 |
| XLOC_009000 | -1.9702840 | 2.1399072 | ||
| RF55_1494 | XP_016771667.1 | -1.8255253 | 2.2245942 | |
| RF55_2964 | GB45277 | multidrug resistance-associated protein 4-like | -1.9410464 | 2.0992859 |
| RF55_13040 | XP_016771370.1 | -1.7071168 | 2.3051344 | |
| XLOC_009717 | -1.8567534 | 2.1300834 | ||
| RF55_6105 | GB40496 | aftiphilin-like | -1.9290288 | 2.0409600 |
| RF55_2225 | XP_016769102.1 | -2.4576563 | 1.5031576 | |
| RF55_7166 | GB51290 | ultrabithorax | -1.8574204 | 2.0948477 |
| RF55_2340 | GB55485 | DNA methyltransferase 3 | -2.2221680 | 1.7086023 |
| RF55_5141 | GB51219 | eye-specific diacylglycerol kinase | -1.5771776 | 2.3341264 |
| RF55_3424 | GB42681 | mucin-5AC-like | -1.9129112 | 1.9909363 |
| RF55_335 | GB42666 | serine palmitoyltransferase 2-like | -2.1856978 | 1.6894768 |
| RF55_2921 | GB40416 | twist | -2.1419203 | 1.6755463 |
| RF55_1441 | GB47599 | cytoplasmic dynein 1 light intermediate chain 1 | -1.3649356 | 2.3461757 |
| XLOC_001241 | -1.9132811 | 1.7758352 | ||
| RF55_404 | GB53011 | polyphosphoinositide phosphatase | -2.1273247 | 1.5615310 |
| RF55_11430 | XP_016769030.1 | -2.0923206 | 1.5691347 | |
| RF55_1609 | GB40975 | gamma-aminobutyric acid receptor subunit beta | -1.9326037 | 1.6691322 |
| RF55_5498 | GB55971 | palmitoyltransferase ZDHHC9-like | -1.8138672 | 1.6963432 |
| RF55_13282 | GB54319 | synaptotagmin 20 | -1.8203872 | 1.6560353 |
| RF55_4134 | XP_016771187.1 | -1.6338628 | 1.7842745 | |
| RF55_3869 | GB51413 | C3 and PZP-like alpha-2-macroglobulin domain-containing protein 8-like | -1.8352815 | 1.5643281 |
| RF55_5507 | XP_016772718.1 | -1.5504913 | 1.7564732 | |
| RF55_3824 | XP_016768669.1 | -1.5248764 | 1.6085396 | |
| XLOC_005436 | -1.7586500 | 1.3642664 | ||
| RF55_10519 | GB54446 | arginine kinase | -2.9654802 | 0.1456319 |
| RF55_310 | 100576851 | ornithine decarboxylase antizyme 1-like | -2.1712838 | 0.4835235 |
| RF55_3137 | GB54056 | serine hydroxymethyltransferase, cytosolic | -0.5039290 | 0.3060241 |
| RF55_6300 | XP_016767697.1 | -0.1938198 | 0.3975841 | |
| RF55_4024 | XP_016767817.1 | -0.2959092 | 0.2953227 |
find.alternatively.spliced.genes("bt")
## [1] Gene Name Lowest FC Highest FC
## <0 rows> (or 0-length row.names)
lf.alt <- lf.alt.splice$Name[lf.alt.splice$Name != " "] # Exclude genes with no A. mellifera names
ln.alt <- ln.alt.splice$Name[ln.alt.splice$Name != " "]
venn(list(Apis = am.alt.splice$Name,`L. flavus` = lf.alt,`L. niger` = ln.alt))
First, we define a series of functions for gene co-expression network analysis.
# This function uses the ComBat function from the package 'sva' to remove variance in gene expression
# that is due to colony and species, allowing us to detect variance due to queen pheromone treatment.
# The use of ComBat in this fashion follows recommendations from the author of the WGCNA package.
remove.effects.combat <- function(expression.data){
sampleIDs <- rownames(expression.data)
ids <- with(treatments[match(sampleIDs, treatments$id), ],
data.frame(
id = sampleIDs,
species = species,
treatment = treatment,
colony = paste(species, colony, sep = "")))
modcombat <- model.matrix(~as.factor(treatment), data=ids)
shh <- capture.output(expression.data <- ComBat(dat = t(expression.data),
batch = ids$species,
mod = modcombat,
par.prior = TRUE))
shh <- capture.output(expression.data <- t(ComBat(dat = expression.data,
batch = ids$colony,
mod = modcombat,
par.prior = TRUE)))
list(expression.data, ids)
}
# Build a gene coexpresison network using WGCNA package
build.network <- function(expression.data.list){
# Pick the soft thresholding power that gives a model fit of R^2 > 0.8 for the scale-free topology model
soft.power <- pickSoftThreshold(expression.data.list[[1]],
RsquaredCut = 0.8, verbose = 0, powerVector = 1:30)
# Use this power to generate a gene co-expression network, using the default settings
network <- blockwiseModules(expression.data.list[[1]],
power = soft.power$powerEstimate,
networkType = "signed",
minModuleSize = 30,
verbose = 0,
saveTOMs = T)
list(network, expression.data.list[[2]])
}
# By default, WGCNA gives the transcriptional modules random names like 'turqoise' or 'darkred'.
# I think it's more helpful to define the biggest module as 'Module 1', the second biggest as 'Module 2', etc
# I use the label 'Module 0' for genes that were not assigned to a module
convert.module.colors.to.names <- function(network){
module.sizes <- table(network[[1]]$colors) %>% sort %>% rev
module.sizes <- c(module.sizes[names(module.sizes) == "grey"],
module.sizes[names(module.sizes) != "grey"])
module.mappings <- data.frame(color = names(module.sizes),
new.name = paste("Module",
0:(length(module.sizes)-1)), stringsAsFactors = F)
network[[1]]$colors <- module.mappings$new.name[match(network[[1]]$colors, module.mappings$color)]
names(network[[1]]$MEs) <- gsub("ME", "", names(network[[1]]$MEs))
names(network[[1]]$MEs) <- module.mappings$new.name[match(names(network[[1]]$MEs),
module.mappings$color)]
network
}
# Rearrange the data in a handy format for stats and plotting, and remove the 'Module 0', the un-assigned genes
rearrange.eigengene.data <- function(network.list){
cbind(network.list[[2]], network.list[[1]]$MEs) %>%
gather(Module, Eigengene, starts_with("Module")) %>%
filter(Module != "Module 0") %>%
rename(Species = species, Treatment = treatment) %>%
arrange(Species, Treatment, colony, Module)
}
# Run a model selection analysis on each module. The full linear model has eigengene as the response variable, and treatment, species and treatment:species as predictors. We rank the 5 possible models using their AIC scores, and test which provides the best fit to the data (the 'delta' and 'weight' parameters reveal the difference in explantory power)
run.stats <- function(dat){
do.one.module <- function(module, dat){
options(na.action = "na.fail") # need to set this option when running dredge()
full.model <- lm(Eigengene ~ Treatment * Species,
data = dat[dat$Module == paste("Module", module), ])
output <- suppressMessages(dredge(full.model)) # compare full model and the four possible simpler models
options(na.action = "na.omit") # set it back to default
cbind(Module = module, output %>% as.data.frame()) # Add the module name to the results
}
stats <- do.call("rbind", # Run model selection on every module
lapply(1:length(unique(eigen.data$Module)), do.one.module, eigen.data))
stats[,names(stats) %in% c("logLik", "AICc", "delta", "weight")] <-
format(round(stats[,names(stats) %in% c("logLik", "AICc", "delta", "weight")], 2), nsmall = 2) # rounding
rownames(stats) <- NULL
stats <- stats[,-2] # Remove the intercept column
stats$Module[duplicated(stats$Module)] <- " "
model <- rep("Null model")
model[stats$Species == "+"] <- "~ Species"
model[stats$Treatment == "+"] <- "~ Treatment"
model[stats$Species == "+" & stats$Treatment == "+"] <- "~ Species + Treatment"
model[stats$`Species:Treatment` == "+"] <- "~ Species x Treatment"
model[is.na(model)] <- "Null model"
stats <- with(stats, data.frame(Module, Model = model,
stats[,names(stats) %in% c("logLik", "AICc", "delta", "weight")]))
stats
}
# The 4 bad samples get removed, then we find the orthologous genes, the data are scaled with ComBat, and then we build the network using the lowest soft-thresholding power that gives at least R^2 > 0.8 model fit
OGGs <- make.OGGs(c("am", "bt", "ln", "lf"), bad.samples = bad.samples)
network <- OGGs[[1]] %>%
remove.effects.combat() %>%
build.network() %>%
convert.module.colors.to.names()
eigen.data <- network %>% rearrange.eigengene.data
Here is the number of orthologous genes that form the network:
length(network[[1]]$colors)
## [1] 3465
Here is the number and size of modules in the network - module 0 refers to the unassigned genes.
table(network[[1]]$colors) %>% pander
| Module 0 | Module 1 | Module 2 | Module 3 | Module 4 | Module 5 | Module 6 |
|---|---|---|---|---|---|---|
| 107 | 1639 | 543 | 346 | 288 | 160 | 154 |
| Module 7 | Module 8 | Module 9 |
|---|---|---|
| 150 | 40 | 38 |
# Make a plot of the module eigengenes, split by species, module and treatment
treatments.network.plot <- function(dat){
dat %>% mutate(Treatment = replace(as.character(Treatment), Treatment == "QP", "Queen\npheromone")) %>%
ggplot(aes(Species, Eigengene, fill = Treatment)) +
geom_hline(yintercept = 0, linetype=2) +
geom_boxplot() +
facet_wrap(~Module) +
xlab(NULL) +
scale_x_discrete(labels = c("Apis\nmellifera", "Bombus\nterrestris", "Lasius\nflavus", "Lasius\nniger")) +
scale_fill_brewer(name = " ", palette = "Set3", direction = -1) +
theme_bw() +
theme(strip.background = element_blank(),
axis.text.x = element_text(face = "italic"),
panel.border = element_rect(size=0.7),
legend.position = "top")
}
eigen.data %>% treatments.network.plot()
ggsave(eigen.data %>% treatments.network.plot(),
file = "figures/Module eigengenes.pdf", height = 6.6, width = 8)
Figure 4: The figure shows the distribution of module eigengenes for each combination of module, species, and queen pheromone (QP) treatment. Positive values mean that the focal group has higher eigengenes, which derived from the relative expression levels of a module of genes, than the average.
Table S13: Model selection analysis, using AICc (corrected Akaike Information Criterion) to rank all possible models of the module eigengene data shown in Figure S5. The models are listed from best to worst for each module. The ‘delta’ column gives the difference in AICc scores between the focal model and the top model in the set, where delta > 2 is considered to be a significant improvement in model fit. The column ‘weight’ gives Akaike weights, which can be interpreted as probabilities that the focal model is the top model in the set, given the data.
run.stats(eigen.data) %>% kable.table()
| Module | Model | logLik | AICc | delta | weight |
|---|---|---|---|---|---|
| 1 | ~ Treatment | 17.71 | -28.74 | 0.00 | 0.59 |
| Null model | 16.10 | -27.87 | 0.87 | 0.38 | |
| ~ Species + Treatment | 17.72 | -20.81 | 7.93 | 0.01 | |
| ~ Species | 16.10 | -20.39 | 8.35 | 0.01 | |
| ~ Species x Treatment | 20.71 | -17.22 | 11.52 | 0.00 | |
| 2 | ~ Treatment | 17.28 | -27.88 | 0.00 | 0.49 |
| Null model | 16.10 | -27.87 | 0.01 | 0.49 | |
| ~ Species | 16.10 | -20.39 | 7.49 | 0.01 | |
| ~ Species + Treatment | 17.29 | -19.95 | 7.93 | 0.01 | |
| ~ Species x Treatment | 19.39 | -14.57 | 13.31 | 0.00 | |
| 3 | Null model | 16.10 | -27.87 | 0.00 | 0.50 |
| ~ Treatment | 17.24 | -27.79 | 0.08 | 0.48 | |
| ~ Species | 16.11 | -20.39 | 7.47 | 0.01 | |
| ~ Species + Treatment | 17.24 | -19.85 | 8.02 | 0.01 | |
| ~ Species x Treatment | 21.01 | -17.82 | 10.05 | 0.00 | |
| 4 | ~ Treatment | 26.92 | -47.15 | 0.00 | 0.92 |
| ~ Species x Treatment | 33.05 | -41.89 | 5.27 | 0.07 | |
| ~ Species + Treatment | 26.92 | -39.22 | 7.93 | 0.02 | |
| Null model | 16.10 | -27.87 | 19.28 | 0.00 | |
| ~ Species | 16.11 | -20.40 | 26.75 | 0.00 | |
| 5 | Null model | 16.10 | -27.87 | 0.00 | 0.60 |
| ~ Treatment | 16.77 | -26.86 | 1.01 | 0.37 | |
| ~ Species | 16.10 | -20.39 | 7.48 | 0.01 | |
| ~ Species x Treatment | 21.77 | -19.33 | 8.53 | 0.01 | |
| ~ Species + Treatment | 16.78 | -18.93 | 8.94 | 0.01 | |
| 6 | Null model | 16.10 | -27.87 | 0.00 | 0.70 |
| ~ Treatment | 16.13 | -25.57 | 2.30 | 0.22 | |
| ~ Species x Treatment | 23.61 | -23.00 | 4.86 | 0.06 | |
| ~ Species | 16.11 | -20.40 | 7.47 | 0.02 | |
| ~ Species + Treatment | 16.13 | -17.64 | 10.23 | 0.00 | |
| 7 | Null model | 16.10 | -27.87 | 0.00 | 0.74 |
| ~ Treatment | 16.17 | -25.65 | 2.22 | 0.24 | |
| ~ Species | 16.11 | -20.39 | 7.48 | 0.02 | |
| ~ Species + Treatment | 16.17 | -17.72 | 10.15 | 0.00 | |
| ~ Species x Treatment | 16.40 | -8.59 | 19.27 | 0.00 | |
| 8 | Null model | 16.10 | -27.87 | 0.00 | 0.68 |
| ~ Treatment | 16.44 | -26.20 | 1.67 | 0.29 | |
| ~ Species | 16.28 | -20.75 | 7.12 | 0.02 | |
| ~ Species + Treatment | 16.63 | -18.64 | 9.23 | 0.01 | |
| ~ Species x Treatment | 17.98 | -11.75 | 16.12 | 0.00 | |
| 9 | ~ Treatment | 18.42 | -30.15 | 0.00 | 0.74 |
| Null model | 16.10 | -27.87 | 2.29 | 0.24 | |
| ~ Species + Treatment | 18.42 | -22.22 | 7.93 | 0.01 | |
| ~ Species | 16.11 | -20.39 | 9.76 | 0.01 | |
| ~ Species x Treatment | 19.58 | -14.96 | 15.19 | 0.00 |
meta.module.plot <- function(network){
MET <- network[[1]]$MEs
MET <- data.frame(QP = (network[[2]]$treatment %>% as.numeric())-1, MET) %>% dplyr::select(-Module.0)
names(MET) <- gsub("[.]", " ", names(MET))
cluster <- (1 - cor(MET)) %>% as.dist() %>% hclust()
ordering <- cluster$labels[cluster$order]
heat.map.data <- cor(MET) %>% melt %>%
mutate(Var1 = factor(Var1, levels = ordering),
Var2 = factor(Var2, levels = ordering)) %>%
rename(Corr = value)
heat.map <- heat.map.data %>% ggplot(aes(Var1, Var2, fill = Corr)) + geom_tile() +
scale_fill_gradient2(low = brewer.pal(9, "RdBu")[8],
mid = "white",
high = brewer.pal(9, "RdBu")[2]) +
xlab(NULL) + ylab(NULL) +
theme_bw() +
theme(panel.border = element_blank(),
panel.grid = element_blank()) +
scale_x_discrete(expand = c(0,0)) +
scale_y_discrete(expand = c(0,0))
dendrogram <- ggdendrogram(cluster) + theme(axis.text.x = element_blank(), axis.text.y = element_blank())
p1 <- grid.arrange(dendrogram, heat.map)
invisible(p1)
}
meta.plot <- meta.module.plot(network)
ggsave(meta.plot, file = "figures/meta_module_heat_map.pdf", width = 5, height = 7.3, units = "in")
meta.plot
## TableGrob (2 x 1) "arrange": 2 grobs
## z cells name grob
## 1 1 (1-1,1-1) arrange gtable[layout]
## 2 2 (2-2,1-1) arrange gtable[layout]
Figure S5: Dendrogram and heat map showing the correlations among module eigengene values and the queen pheromone treatment (QP; coded as zero and 1 for the control and treatment respectively). Modules with red colour, or which are close on the dendrogram, show more correlated expression. The queen pheromone treatment was correlated with Module 5, but was relatively uncorrelated with the other modules.
Table S13: Results of Spearman’s rank correlations testing for a relationship between the effect of queen pheromone on gene expression, and the connectedness of the gene. Negative values of Spearman’s Rho mean that highly pheromone-sensitive genes tend to have lower connectedness.
load("blockwiseTOM-block.1.RData") # Load the TOM from the network analysis - can be used to find connectedness for each ortholog
# Get the phermonone sensitivity value for each of the OGGs, and line it up with the connectedness data
suppressMessages(dd <- OGGs[[2]] %>% left_join(tbl(my_db, "ebseq_gene_am") %>% select(gene, PostFC) %>% rename(am=gene), copy=T) %>% rename(am_FC = PostFC) %>%
left_join(tbl(my_db, "ebseq_gene_bt") %>% select(gene, PostFC) %>%
rename(bt=gene), copy=T) %>% rename(bt_FC = PostFC) %>%
left_join(tbl(my_db, "ebseq_gene_lf") %>% select(gene, PostFC) %>%
rename(lf=gene), copy=T) %>% rename(lf_FC = PostFC) %>%
left_join(tbl(my_db, "ebseq_gene_ln") %>% select(gene, PostFC) %>%
rename(ln=gene), copy=T) %>% rename(ln_FC = PostFC) %>%
mutate(k = colSums(as.matrix(TOM))))
do.spearman <- function(dd, species, name){ # run spearman on each species
test <- cor.test(dd$k, dd[, names(dd) == species] %>% log2 %>% abs, method = "spearman") # Note that we convert the fold-change in expression with abs(log2(x)), to get pheromone sensitivity
with(test, data.frame(Species = name, rho = estimate, p = p.value, row.names = NULL))
}
suppressWarnings(results <- rbind(do.spearman(dd, "am_FC", "Apis mellifera"),
do.spearman(dd, "bt_FC", "Bombus terrestris"),
do.spearman(dd, "lf_FC", "Lasius flavus"),
do.spearman(dd, "ln_FC", "Lasius niger")))
rownames(results) <- NULL
pander(results)
| Species | rho | p |
|---|---|---|
| Apis mellifera | -0.2463 | 4.834e-49 |
| Bombus terrestris | -0.2988 | 2.076e-72 |
| Lasius flavus | -0.4151 | 1.854e-144 |
| Lasius niger | -0.3159 | 4.677e-81 |
In this section, we search for correlates of the absolute Log_2 fold change in response to pheromone (where positive values denote genes whose expression differs strongly between the control and pheromone treatment). This section makes use of data kindly provided by Soojin Yi and Brendan Hunt.
The data on queen and worker-specific gene expression come from Grozinger et al. 2007. We found that pheromone-sensitive genes tend to be over-expressed by queens relative to sterile workers. However, genes that are over-expressed by fertile workers relative to sterile workers did not tend to be more (or less) pheromone-sensitive.
The methylation level (i.e. % methylated cytosines) data come from Galbraith et al. 2016 (provided by Soojin Yi). We found a negative correlation between methylation and pheromone-sensitivity, suggesting that pheromone-sensitive genes are hypomethylated.
The CpG O/E values were calculated for the latest A. mellifera genome annotation. We found a positive correlation between CpG O/E and pheromone-sensitivity. High CpG is associated with lower rate of DNA methylation, again suggesting that pheromone-sensitive genes are hypomethylated.
The estimates of \(\gamma\), a measure of positive and negative selection similar to dN/dS, come from Harpur et al. 2014 PNAS. There was a significant positive correlation between \(\gamma\) and sensitivity to queen pheromone, suggesting that highly pheromone-sensitive genes tend to be positively selected.
The Codon adaptation index was calculated by Brendan Hunt. A high codon adaptation index denotes high codon usage bias, i.e. where certain synonymous codons are more common than others. Pheromone-sensitive genes showed low codon usage bias.
Lastly, ‘expression level’ refers to the average expression of each gene, expressed as TPM (transcripts per million) as measured by the software RSEM in the present study. Highly expressed genes tended to be less pheromone-sensitive.
# import and clean up the data provided by Brendan Hunt
hunt.data <- read.delim("data/apis_gene_comparisons/Amel_AllData_012709.txt",
header=T, stringsAsFactors = FALSE) %>%
mutate(log2RW.SW = log2(RW_bagel / SW_bagel)) # calculate log fold difference in gene expression between fertile and sterile workers
entrez.tbl <- read.delim("data/apis_gene_comparisons/am.gene_info.txt", stringsAsFactors = FALSE)[,c(2,5,6)] # import table of gene names (Entrez, old Beebase, and new Beebase)
names(entrez.tbl) <- c("entrez.id", "beebase1", "beebase2")
hunt.data <- hunt.data %>%
dplyr::select(ID, log2Q.SW, log2RW.SW, CAI, cpgOE) %>% # get gene ID and the relevant data
rename(beebase1 = ID) %>% # merge based on beebase IDs
left_join(entrez.tbl, by = "beebase1") %>%
filter(!is.na(beebase2) & beebase2 != "-") %>%
mutate(beebase2 = gsub("BEEBASE:", "", beebase2)) %>%
rename(gene = beebase2) %>%
dplyr::select(gene, log2Q.SW, log2RW.SW, CAI, cpgOE)
hunt.data <- left_join(tbl(my_db, "ebseq_gene_am") %>% # merge Hunt's data with our phermone sensitivity data
dplyr::select(gene, PostFC) %>% collect(), hunt.data, by = "gene") %>%
left_join(tbl(my_db, "bee_names") %>% collect, by = "gene") # also add the gene names
# Import methylation data provided by Soojin Yi and Xin Wu (from Galbraith et al PNAS)
methylation <- read.csv("data/apis_gene_comparisons/apis_gene_methyl_CG_OE.csv", stringsAsFactors = FALSE)
methylation <- tbl(my_db, "ebseq_gene_am") %>% collect %>% left_join(methylation, by = "gene") %>%
filter(!is.na(Gene_body_methylation)) %>%
left_join(tbl(my_db, "bee_names") %>% collect(), by = "gene") %>% distinct(gene, .keep_all = T)
# Import gamma data from Harpur et al PNAS
gamma_am <- tbl(my_db, "ebseq_gene_am") %>% collect() %>%
left_join(read.table("data/apis_gene_comparisons/harpur_etal_gamma.txt", header=TRUE, stringsAsFactors=FALSE) %>% rename(gene = Gene), by = "gene") %>%
filter(!is.na(gamma)) %>%
dplyr::select(gene, PostFC, gamma) %>%
mutate(PostFC = log2(PostFC)) %>% left_join(tbl(my_db, "bee_names"), copy=TRUE, by = "gene") %>%
arrange(-abs(PostFC))
merged <- hunt.data %>% dplyr::select(gene, PostFC, log2Q.SW, log2RW.SW, CAI) %>%
left_join(methylation %>% dplyr::select(gene, CG_OE, Gene_body_methylation), by = "gene") %>% # merge in methylation data provided by Soojin Yi
left_join(gamma_am %>% dplyr::select(gene, gamma), by = "gene") %>% # merge in gamma data from Harpur et al
left_join(data.frame(gene = tbl(my_db, "rsem_am") %>%
dplyr::select(gene) %>% collect(), # calculate overall expression level from our own data
expression.level = (tbl(my_db, "rsem_am") %>%
dplyr::select(-gene) %>%
collect %>% rowSums())), by = "gene") %>%
left_join(dd %>% dplyr::select(am, k) %>% rename(gene=am), by = "gene") %>%
dplyr::select(-gene) %>%
mutate(CG_OE = -log2(CG_OE), # log2 CpG O/E ratio - change the sign, so that high values mean high methylation
expression.level = log10(expression.level), # log10 the expression level
PostFC = abs(log2(PostFC))) %>% # absolute log2 fold-change in response to pheromones (i.e. 'pheromone sensitivity' score)
as.data.frame()
m.rename <- function(merged, col, new) {names(merged)[names(merged) == col] <- new; merged}
merged <- merged %>% m.rename("PostFC", "Pheromone sensitivity\n(absolute log fold)") # re-label all the variables nicely
merged <- merged %>% m.rename("log2Q.SW", "Upregulation in queens\n(log fold)")
merged <- merged %>% m.rename("log2RW.SW", "Upregulation in fertile\nworkers (log fold)")
merged <- merged %>% m.rename("CAI", "Codon usage bias\n(CAI)")
merged <- merged %>% m.rename("CG_OE", "DNA methylation\n(CpG depletion)")
merged <- merged %>% m.rename("Gene_body_methylation", "DNA methylation\n(BiS-seq)")
merged <- merged %>% m.rename("gamma", "Positive selection\n(Gamma)")
merged <- merged %>% m.rename("expression.level", "Log Expression level")
merged <- merged %>% m.rename("k", "Connectivity in the\ntranscriptome")
reorder_cormat <- function(cormat){ # reorder a correlation matrix using hierarchical clustering
dd <- as.dist((1-cormat)/2)
hc <- hclust(dd)
cormat[hc$order, hc$order]}
cormat <- reorder_cormat(cor(merged, use = 'pairwise.complete.obs'))
cormat[upper.tri(cormat)] <- NA
diag(cormat) <- NA
cor.matrix <- (melt(cormat) %>% filter(!is.na(value)))[,1:2] %>% mutate(cor=0,p=0)
for(i in 1:nrow(cor.matrix)) cor.matrix[i, 3:4] <- cor.test(merged[, names(merged) == cor.matrix$Var1[i]], merged[, names(merged) == cor.matrix$Var2[i]])[c(4,3)] %>% unlist
cor.matrix$p <- p.adjust(cor.matrix$p, method = "BH") # apply B-H p value correction
cor.matrix$sig <- ""
cor.matrix$sig[cor.matrix$p < 0.05] <- "*"
cor.matrix$sig[cor.matrix$p < 0.001] <- "**"
cor.matrix$sig[cor.matrix$p < 0.0001] <- "***"
cor.matrix$label <- paste(format(round(cor.matrix$cor,2), nSmall =2), cor.matrix$sig)
correlation.plot <- cor.matrix %>%
ggplot(aes(Var1, Var2, fill=cor)) +
geom_tile(colour="grey10",alpha=0.7) +
scale_fill_gradient2(name = "Corr",
low = brewer.pal(9, "RdYlBu")[7],
mid = "white",
high = brewer.pal(9, "RdYlBu")[2]) +
geom_text(aes(label = label), colour = "grey25", size = 3.5) +
xlab(NULL) + ylab(NULL) +
scale_x_discrete(expand=c(0,0)) + scale_y_discrete(expand=c(0, 0)) +
theme_minimal() + theme(axis.text.x = element_text(angle = 45, hjust = 1, face = c("bold", rep("plain", 5), "bold", "plain")),
axis.text.y = element_text(face = c("plain", "bold", rep("plain", 5), "bold")),
panel.grid = element_blank(),
legend.position = "none")
ggsave(correlation.plot, file = "figures/correlation_plot.pdf", width =8, height = 8)
correlation.plot
Figure 5: Correlations across genes between various parameters, for Apis mellifera. ‘Pheromone sensitivity’ was calculated as the absolute value of the Log\(_2\) fold difference in expression between pheromone treatment and the control. The Log FC (fold change) data come from Grozinger et al. 2007 (Mol. Ecol.), and positive values denote genes that have higher expression in queens or fertile workers, relative to sterile workers. Codon usage bias was estimated by the codon adaptation index: high values indicate bias for particular synonymous codons. DNA methylation rate was estimated either by the frequency of CpGs (i.e. -log CpG O/E ratio), or from bisulphite sequencing (BiS-seq). The parameter gamma (\(\gamma\)) describes the form of selection, where positive values denote positive selection, and negative values purifying selection. Lastly, the expression level was calculated from our own dataset as the log transcripts per million, averaged across our 6 Apis libraries.
Morandin et al. 2016 (Genome Biology 17:43) studied whole transcriptomes from queens and workers in 16 diverse ant species, including two other species from the genus Lasius. Using BLAST, they grouped genes into OGGs (orthologous gene groups), and built a co-expression network using all the OGGs that were common to all 16 species (similar to the present study). Their analysis yielded 36 modules, of which many showed significant queen-worker differences in their module eigengenes. Here, we want to test whether these queen- and worker-like modules significantly overlap with the pheromone-sensitive modules in the present study.
To do this, we used BLAST to identify orthologous gens in L. niger and L. flavus that belong to one of Morandin et al.’s OGGs. We then tested for significantly-greater-than-random overlap between Morandin et al’s modules, and our own study’s modules, using hypergeometric tests.
Of all the possible module pairs, we found 6 pairs that overlapped significantly more than expected (FDR-corrected). One of these pairs included our highly pheromone-sensitive module, Module 4, which overlapped with the caste-biased Module 13 from Morandin et al. The intersecting genes include protein take-out like, a NAD kinase 2, a serine protease, and histone H2A-like.
Table S14: A list of the six module pairs, from Morandin et al. 2016 and the present study, which had significantly more genes in common than expected by chance. The p-values were calculated by running hypergeometric tests on all possible pairs of modules from the two studies, and then adjusting all the p-values using the Benjamini-Hochberg procedure.
morandin.orthology <- read.csv("data/morandin_comparison_data/Morandin to Holman orthology.csv", stringsAsFactors = FALSE)
morandin.module.membership <- read.csv("data/morandin_comparison_data/Morandin module membership.csv", stringsAsFactors = FALSE)
morandin.module.caste.bias <- read.csv("data/morandin_comparison_data/Morandin module caste bias.csv", stringsAsFactors = FALSE)
# Create list of all the L. niger & L. flavus genes are are part of
# the Orthologous Gene Groups (OGGs) from Morandin et al.
# Here are the 3634 genes for which we have 1-to-1 orthologs in all 18 species:
morandin.oggs <- make.OGGs(c("ln", "lf"))[[2]] %>%
left_join(morandin.orthology, by = "ln") %>%
filter(!is.na(morandin.ogg)) %>%
left_join(morandin.module.membership, by = "morandin.ogg") %>%
left_join(tbl(my_db, "ln2am") %>%
left_join(tbl(my_db, "bee_names"), by = c("am" = "gene")) %>%
filter(!is.na(name)) %>% select(ln, name, am) %>%
rename(apis.name = name) %>% collect(n=Inf), by = "ln") %>%
left_join(morandin.module.caste.bias, by = "module") %>%
rename(morandin.module = module) %>%
left_join(data.frame(ln = OGGs[[2]]$ln,
holman.module = network[[1]]$colors,
stringsAsFactors = F), by = "ln") %>%
left_join(tbl(my_db, "ebseq_gene_ln") %>%
select(gene, PostFC) %>% collect(n=Inf) %>% rename(ln = gene), by = "ln") %>%
rename(FC.pheromone = PostFC)
overlaps <- table(morandin.oggs$morandin.module,
morandin.oggs$holman.module) %>%
melt() %>% rename(morandin.module = Var1,
holman.module = Var2,
overlaps = value) %>%
filter(holman.module != "Module 0") %>%
left_join(table(morandin.oggs$morandin.module) %>%
melt() %>% rename(mor.mod.size = value),
by = c("morandin.module" = "Var1")) %>%
left_join(table(morandin.oggs$holman.module) %>% melt() %>%
rename(hol.mod.size = value), by = c("holman.module" = "Var1"))
# List all the Morandin et al. modules that significantly overlap with our own modules
overlaps <- data.frame(
overlaps,
do.call("rbind",
lapply(1:nrow(overlaps),
function(i) with(overlaps,
overlap.hypergeometric.test(
overlaps[i],
mor.mod.size[i],
hol.mod.size[i],
nrow(morandin.oggs),
species = "xx"))))[,2:3]) %>%
filter(Test == "Overlap is higher than expected:") %>%
arrange(p) %>% select(-Test) %>%
left_join(morandin.oggs %>%
select(morandin.module, caste.bias) %>%
distinct(), by = "morandin.module") %>%
mutate(p = p.adjust(p, method = "BH"),
morandin.module = paste("Module", morandin.module)) %>%
filter(p < 0.05)
names(overlaps) <- c("Morandin module", "Holman module", "n overlapping genes", "Size of Morandin module", "Size of Holman module", "p-value", "Caste bias of Morandin module")
overlaps %>%
pander(split.cell = 40, split.table = Inf)
| Morandin module | Holman module | n overlapping genes | Size of Morandin module | Size of Holman module | p-value | Caste bias of Morandin module |
|---|---|---|---|---|---|---|
| Module 32 | Module 2 | 20 | 39 | 363 | 8.886e-09 | Worker-biased |
| Module 31 | Module 1 | 69 | 161 | 969 | 0.0002602 | Queen-biased |
| Module 26 | Module 8 | 5 | 49 | 24 | 0.0005457 | Worker-biased |
| Module 32 | Module 8 | 4 | 39 | 24 | 0.003328 | Worker-biased |
| Module 13 | Module 4 | 10 | 61 | 177 | 0.01554 | Queen-biased |
| Module 10 | Module 3 | 10 | 77 | 150 | 0.02318 | Worker-biased |
A list of the genes (OGGs) that appear in the present study’s Module 4 (which is pheromone-sensitive), and also in Morandin et al.’s Module 13 (which is caste-biased).
morandin.oggs %>%
filter(morandin.module == 13, holman.module == "Module 4") %>%
.$apis.name
## [1] "tumor suppressor candidate 3-like"
## [2] "methyltransferase-like isoform X3"
## [3] "uncharacterized protein LOC726417"
## [4] "uncharacterized protein LOC100576236 isoform X1"
## [5] "NAD kinase 2, mitochondrial-like"
## [6] "histone H2A-like"
## [7] "protein takeout-like"
## [8] "uncharacterized protein LOC551133 isoform X2"
## [9] "xenotropic and polytropic retrovirus receptor 1 homolog"
## [10] "putative serine protease K12H4.7-like isoform X2"
First, define some functions we will need. See also the R script “Script to set up for GO analyses.R”, which was used to make the object gene_set_collection.RData, following instructions for making a GO annotation for a non-model organism at http://bioconductor.org/packages/2.11/bioc/vignettes/GOstats/inst/doc/GOstatsForUnsupportedOrganisms.pdf.
There are only two differentially expressed genes for B. terrestris, so it is only meaningful to test for enriched GO/KEGG terms in the other three species.
GO.and.KEGG.enrichment <- function(enriched.genes, gene.universe, kable = TRUE, keep.all = FALSE){
p <- 0.05
neatness <- function(x, dp) format(round(x, dp), nsmall = 3)
if(keep.all) p <- 1
GO.enrichment <- function(enriched.genes, gene.universe, ontology){
params <- GSEAGOHyperGParams(
name = "Luke's Params",
geneSetCollection = gene_set_collection, # custom GO annotations
geneIds = enriched.genes,
universeGeneIds = gene.universe,
ontology = ontology, # Can be BP, MF, or CC
pvalueCutoff = p,
conditional = TRUE, # Do the test conditional on the GO structure
testDirection = "over") # Look for over-represented GO terms, not under
output <- hyperGTest(params) %>%
summary() %>%
dplyr::mutate(Pvalue = neatness(Pvalue, 5),
OddsRatio = neatness(OddsRatio, 3),
ExpCount = neatness(ExpCount, 3))
names(output)[1] <- "ID"
type <- "Biological process"
if(ontology == "MF") type <- "Molecular function"
if(ontology == "CC") type <- "Cellular component"
if(nrow(output)==0) return(NULL)
data.frame(Test_type = paste("GO", type, sep = ": "), output)
}
kegg.enrichment <- function(enriched.genes, gene.universe){
params <- GSEAKEGGHyperGParams(
name = "Luke's Params",
geneSetCollection = gene_set_collection_kegg, # custom KEGG annotations
geneIds = enriched.genes,
universeGeneIds = gene.universe,
pvalueCutoff = p,
testDirection = "over") # Look for over-represented KEGG terms, not under
output <- hyperGTest(params) %>%
summary() %>%
dplyr::mutate(Pvalue = neatness(Pvalue, 5),
OddsRatio = neatness(OddsRatio, 3),
ExpCount = neatness(ExpCount, 3),
KEGGID = paste("KEGG", KEGGID, sep = ":")) %>%
rename(ID = KEGGID)
data.frame(Test_type = "KEGG", output)
}
output <- rbind(kegg.enrichment(enriched.genes, gene.universe),
GO.enrichment(enriched.genes, gene.universe, "BP"),
GO.enrichment(enriched.genes, gene.universe, "MF"),
GO.enrichment(enriched.genes, gene.universe, "CC"))
if(!kable) return(output)
output %>% kable.table()
}
# Find the names for the genes in a given module
genes.in.module <- function(module.number){
colnames(OGGs[[1]])[network[[1]]$colors == paste("Module", module.number)]
}
# Get the gene names, and sensitivity to pheromone, for genes in a certain module
inspect.module.genes <- function(module){
gene.names <- tbl(my_db, "bee_names") %>% as.data.frame()
gene.names <- gene.names[gene.names$gene %in% genes.in.module(module), ]
gene.names$k <- colSums(as.matrix(TOM)[network[[1]]$colors == paste("Module", module),
network[[1]]$colors == paste("Module", module)])
gene.names <- gene.names %>% arrange(-k)
am <- tbl(my_db, "ebseq_gene_am") %>% as.data.frame()
gene.names$am_fc <- am$PostFC[match(gene.names$gene, am$gene)]
bt <- tbl(my_db, "ebseq_gene_bt") %>% rename(bt = gene) %>%
left_join(tbl(my_db, "bt2am")) %>% as.data.frame()
gene.names$bt_fc <- bt$PostFC[match(gene.names$gene, bt$am)]
lf <- tbl(my_db, "ebseq_gene_lf") %>% rename(lf = gene) %>%
left_join(tbl(my_db, "lf2am")) %>% as.data.frame()
gene.names$lf_fc <- lf$PostFC[match(gene.names$gene, lf$am)]
ln <- tbl(my_db, "ebseq_gene_ln") %>% rename(ln = gene) %>%
left_join(tbl(my_db, "ln2am")) %>% as.data.frame()
gene.names$ln_fc <- ln$PostFC[match(gene.names$gene, ln$am)]
row.names(gene.names) <- NULL
gene.names
}
# Load the gene set collection object needed for the GO tests
load("data/gene_set_collection.RData")
# Load the gene set collection object needed for the KEGG tests
load("data/gene_set_collection_kegg.RData")
Table S15: Results of KEGG and GO enrichment analysis on the list of genes that were significantly upregulated in the control group in A. mellifera. The gene universe was defined as all A. mellifera genes measured in this study.
gene.universe.apis <- (tbl(my_db, "rsem_am") %>%
as.data.frame())$gene
up.in.control.apis <- (apis.de %>% filter(`Log2 FC` > 0) %>% as.data.frame())$Gene
suppressMessages(GO.and.KEGG.enrichment(up.in.control.apis, gene.universe.apis))
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:03010 | 0.00000 | 24.523 | 6.252 | 53 | 121 | Ribosome |
| KEGG | KEGG:03050 | 0.00011 | 5.865 | 2.015 | 9 | 39 | Proteasome |
| KEGG | KEGG:04145 | 0.01426 | 2.787 | 3.255 | 8 | 63 | Phagosome |
| KEGG | KEGG:03060 | 0.01726 | 4.710 | 1.033 | 4 | 20 | Protein export |
| KEGG | KEGG:03013 | 0.04024 | 1.955 | 6.149 | 11 | 119 | RNA transport |
| GO: Biological process | GO:0006518 | 0.00000 | 20.136 | 6.672 | 51 | 175 | peptide metabolic process |
| GO: Biological process | GO:0043604 | 0.00000 | 20.381 | 6.405 | 50 | 168 | amide biosynthetic process |
| GO: Biological process | GO:0006412 | 0.00000 | 21.247 | 5.361 | 45 | 147 | translation |
| GO: Biological process | GO:1901566 | 0.00000 | 12.811 | 10.827 | 56 | 284 | organonitrogen compound biosynthetic process |
| GO: Biological process | GO:0019538 | 0.00000 | 11.237 | 11.290 | 53 | 307 | protein metabolic process |
| GO: Biological process | GO:0009059 | 0.00000 | 4.098 | 21.426 | 51 | 562 | macromolecule biosynthetic process |
| GO: Biological process | GO:0044249 | 0.00000 | 3.392 | 29.203 | 57 | 766 | cellular biosynthetic process |
| GO: Biological process | GO:0034641 | 0.00000 | 3.060 | 33.931 | 60 | 890 | cellular nitrogen compound metabolic process |
| GO: Biological process | GO:0044260 | 0.00000 | 2.998 | 35.303 | 61 | 926 | cellular macromolecule metabolic process |
| GO: Biological process | GO:0071704 | 0.00001 | 2.652 | 55.242 | 76 | 1449 | organic substance metabolic process |
| GO: Biological process | GO:0006414 | 0.00413 | 52.000 | 0.113 | 2 | 3 | translational elongation |
| GO: Biological process | GO:0071826 | 0.01358 | 4.964 | 0.953 | 4 | 25 | ribonucleoprotein complex subunit organization |
| GO: Biological process | GO:0016485 | 0.01953 | 12.852 | 0.229 | 2 | 6 | protein processing |
| GO: Biological process | GO:0006417 | 0.02478 | 5.543 | 0.648 | 3 | 17 | regulation of translation |
| GO: Biological process | GO:0015991 | 0.02478 | 5.543 | 0.648 | 3 | 17 | ATP hydrolysis coupled proton transport |
| GO: Biological process | GO:0019805 | 0.03812 | Inf | 0.038 | 1 | 1 | quinolinate biosynthetic process |
| GO: Biological process | GO:1902001 | 0.03812 | Inf | 0.038 | 1 | 1 | fatty acid transmembrane transport |
| GO: Biological process | GO:0006231 | 0.03812 | Inf | 0.038 | 1 | 1 | dTMP biosynthetic process |
| GO: Biological process | GO:0045900 | 0.03812 | Inf | 0.038 | 1 | 1 | negative regulation of translational elongation |
| GO: Biological process | GO:1903825 | 0.03812 | Inf | 0.038 | 1 | 1 | organic acid transmembrane transport |
| GO: Biological process | GO:0009157 | 0.03812 | Inf | 0.038 | 1 | 1 | deoxyribonucleoside monophosphate biosynthetic process |
| GO: Biological process | GO:0009176 | 0.03812 | Inf | 0.038 | 1 | 1 | pyrimidine deoxyribonucleoside monophosphate metabolic process |
| GO: Biological process | GO:0043420 | 0.03812 | Inf | 0.038 | 1 | 1 | anthranilate metabolic process |
| GO: Biological process | GO:0006069 | 0.03812 | Inf | 0.038 | 1 | 1 | ethanol oxidation |
| GO: Biological process | GO:0034354 | 0.03812 | Inf | 0.038 | 1 | 1 | ‘de novo’ NAD biosynthetic process from tryptophan |
| GO: Biological process | GO:0034308 | 0.03812 | Inf | 0.038 | 1 | 1 | primary alcohol metabolic process |
| GO: Biological process | GO:0000028 | 0.03812 | Inf | 0.038 | 1 | 1 | ribosomal small subunit assembly |
| GO: Biological process | GO:0030163 | 0.04027 | 2.576 | 2.554 | 6 | 67 | protein catabolic process |
| GO: Molecular function | GO:0003735 | 0.00000 | 43.470 | 2.977 | 47 | 107 | structural constituent of ribosome |
| GO: Molecular function | GO:0004298 | 0.00001 | 25.966 | 0.334 | 5 | 12 | threonine-type endopeptidase activity |
| GO: Molecular function | GO:0003723 | 0.00002 | 3.919 | 4.841 | 16 | 178 | RNA binding |
| GO: Molecular function | GO:0005544 | 0.00226 | 71.016 | 0.083 | 2 | 3 | calcium-dependent phospholipid binding |
| GO: Molecular function | GO:0003743 | 0.00394 | 7.188 | 0.668 | 4 | 24 | translation initiation factor activity |
| GO: Molecular function | GO:0019843 | 0.01449 | 14.307 | 0.193 | 2 | 7 | rRNA binding |
| GO: Molecular function | GO:0008097 | 0.02782 | Inf | 0.028 | 1 | 1 | 5S rRNA binding |
| GO: Molecular function | GO:0004799 | 0.02782 | Inf | 0.028 | 1 | 1 | thymidylate synthase activity |
| GO: Molecular function | GO:0051903 | 0.02782 | Inf | 0.028 | 1 | 1 | S-(hydroxymethyl)glutathione dehydrogenase activity |
| GO: Molecular function | GO:0004852 | 0.02782 | Inf | 0.028 | 1 | 1 | uroporphyrinogen-III synthase activity |
| GO: Molecular function | GO:0033925 | 0.02782 | Inf | 0.028 | 1 | 1 | mannosyl-glycoprotein endo-beta-N-acetylglucosaminidase activity |
| GO: Molecular function | GO:0003922 | 0.02782 | Inf | 0.028 | 1 | 1 | GMP synthase (glutamine-hydrolyzing) activity |
| GO: Molecular function | GO:0004502 | 0.02782 | Inf | 0.028 | 1 | 1 | kynurenine 3-monooxygenase activity |
| GO: Molecular function | GO:0004427 | 0.02782 | Inf | 0.028 | 1 | 1 | inorganic diphosphatase activity |
| GO: Molecular function | GO:0004639 | 0.02782 | Inf | 0.028 | 1 | 1 | phosphoribosylaminoimidazolesuccinocarboxamide synthase activity |
| GO: Molecular function | GO:0070273 | 0.02782 | Inf | 0.028 | 1 | 1 | phosphatidylinositol-4-phosphate binding |
| GO: Molecular function | GO:0008609 | 0.02782 | Inf | 0.028 | 1 | 1 | alkylglycerone-phosphate synthase activity |
| GO: Cellular component | GO:0005840 | 0.00000 | 32.684 | 3.774 | 47 | 111 | ribosome |
| GO: Cellular component | GO:0005737 | 0.00000 | 6.991 | 21.385 | 71 | 629 | cytoplasm |
| GO: Cellular component | GO:0043228 | 0.00000 | 8.045 | 11.220 | 51 | 330 | non-membrane-bounded organelle |
| GO: Cellular component | GO:0032991 | 0.00000 | 5.783 | 21.147 | 65 | 622 | macromolecular complex |
| GO: Cellular component | GO:0043229 | 0.00000 | 3.425 | 21.122 | 47 | 664 | intracellular organelle |
| GO: Cellular component | GO:0005622 | 0.00000 | 2.879 | 56.098 | 87 | 1650 | intracellular |
| GO: Cellular component | GO:0015934 | 0.00000 | 49.270 | 0.272 | 5 | 8 | large ribosomal subunit |
| GO: Cellular component | GO:0015935 | 0.00000 | 37.563 | 0.301 | 5 | 9 | small ribosomal subunit |
| GO: Cellular component | GO:0005623 | 0.00000 | 2.355 | 63.340 | 88 | 1863 | cell |
| GO: Cellular component | GO:1905369 | 0.00033 | 10.525 | 0.646 | 5 | 19 | endopeptidase complex |
| GO: Cellular component | GO:0005839 | 0.00068 | 29.521 | 0.201 | 3 | 6 | proteasome core complex |
| GO: Cellular component | GO:0022627 | 0.00115 | Inf | 0.068 | 2 | 2 | cytosolic small ribosomal subunit |
| GO: Cellular component | GO:0030529 | 0.00832 | 4.415 | 1.275 | 5 | 58 | intracellular ribonucleoprotein complex |
| GO: Cellular component | GO:0019773 | 0.02153 | 11.532 | 0.238 | 2 | 7 | proteasome core complex, alpha-subunit complex |
| GO: Cellular component | GO:0033179 | 0.02153 | 11.532 | 0.238 | 2 | 7 | proton-transporting V-type ATPase, V0 domain |
| GO: Cellular component | GO:0016607 | 0.03400 | Inf | 0.034 | 1 | 1 | nuclear speck |
| GO: Cellular component | GO:0030014 | 0.03400 | Inf | 0.034 | 1 | 1 | CCR4-NOT complex |
| GO: Cellular component | GO:0044446 | 0.04093 | 1.573 | 15.911 | 23 | 468 | intracellular organelle part |
| GO: Cellular component | GO:0016469 | 0.04614 | 4.134 | 0.816 | 3 | 24 | proton-transporting two-sector ATPase complex |
Table S16: Results of KEGG and GO enrichment analysis on the list of genes that were significantly upregulated in the queen pheromone treatment in A. mellifera. The gene universe was defined as all A. mellifera genes measured in this study.
up.in.QP.apis <- (apis.de %>% filter(`Log2 FC` < 0) %>% as.data.frame())$Gene
GO.and.KEGG.enrichment(up.in.QP.apis, gene.universe.apis)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:00250 | 0.01180 | 14.422 | 0.169 | 2 | 25 | Alanine, aspartate and glutamate metabolism |
| KEGG | KEGG:00630 | 0.01273 | 13.815 | 0.176 | 2 | 26 | Glyoxylate and dicarboxylate metabolism |
| KEGG | KEGG:01200 | 0.02283 | 5.782 | 0.630 | 3 | 93 | Carbon metabolism |
| GO: Biological process | GO:0032273 | 0.01173 | 14.344 | 0.169 | 2 | 17 | positive regulation of protein polymerization |
| GO: Biological process | GO:0051495 | 0.01312 | 13.443 | 0.178 | 2 | 18 | positive regulation of cytoskeleton organization |
| GO: Biological process | GO:0044089 | 0.01457 | 12.647 | 0.188 | 2 | 19 | positive regulation of cellular component biogenesis |
| GO: Biological process | GO:0051130 | 0.01768 | 11.307 | 0.208 | 2 | 21 | positive regulation of cellular component organization |
| GO: Biological process | GO:0043254 | 0.01768 | 11.307 | 0.208 | 2 | 21 | regulation of protein complex assembly |
| GO: Biological process | GO:0001678 | 0.01973 | 103.840 | 0.020 | 1 | 2 | cellular glucose homeostasis |
| GO: Biological process | GO:0006537 | 0.01973 | 103.840 | 0.020 | 1 | 2 | glutamate biosynthetic process |
| GO: Biological process | GO:0033500 | 0.01973 | 103.840 | 0.020 | 1 | 2 | carbohydrate homeostasis |
| GO: Biological process | GO:0043044 | 0.02945 | 51.900 | 0.030 | 1 | 3 | ATP-dependent chromatin remodeling |
| GO: Biological process | GO:0043623 | 0.03256 | 7.932 | 0.287 | 2 | 29 | cellular protein complex assembly |
| GO: Biological process | GO:0015980 | 0.03467 | 7.646 | 0.297 | 2 | 30 | energy derivation by oxidation of organic compounds |
| GO: Biological process | GO:0007050 | 0.03909 | 34.587 | 0.040 | 1 | 4 | cell cycle arrest |
| GO: Biological process | GO:0006388 | 0.03909 | 34.587 | 0.040 | 1 | 4 | tRNA splicing, via endonucleolytic cleavage and ligation |
| GO: Biological process | GO:0090063 | 0.04863 | 25.930 | 0.050 | 1 | 5 | positive regulation of microtubule nucleation |
| GO: Biological process | GO:0031113 | 0.04863 | 25.930 | 0.050 | 1 | 5 | regulation of microtubule polymerization |
| GO: Molecular function | GO:0005242 | 0.00011 | Inf | 0.021 | 2 | 2 | inward rectifier potassium channel activity |
| GO: Molecular function | GO:0004114 | 0.00293 | 32.622 | 0.084 | 2 | 8 | 3’,5’-cyclic-nucleotide phosphodiesterase activity |
| GO: Molecular function | GO:0030246 | 0.00366 | 11.068 | 0.316 | 3 | 30 | carbohydrate binding |
| GO: Molecular function | GO:0015930 | 0.01055 | Inf | 0.011 | 1 | 1 | glutamate synthase activity |
| GO: Molecular function | GO:0016639 | 0.01055 | Inf | 0.011 | 1 | 1 | oxidoreductase activity, acting on the CH-NH2 group of donors, NAD or NADP as acceptor |
| GO: Molecular function | GO:0004108 | 0.01055 | Inf | 0.011 | 1 | 1 | citrate (Si)-synthase activity |
| GO: Molecular function | GO:0022843 | 0.01338 | 13.022 | 0.179 | 2 | 17 | voltage-gated cation channel activity |
| GO: Molecular function | GO:0008081 | 0.02012 | 10.271 | 0.221 | 2 | 21 | phosphoric diester hydrolase activity |
| GO: Molecular function | GO:0004396 | 0.02098 | 95.848 | 0.021 | 1 | 2 | hexokinase activity |
| GO: Molecular function | GO:0005536 | 0.02098 | 95.848 | 0.021 | 1 | 2 | glucose binding |
| GO: Molecular function | GO:0022832 | 0.02592 | 8.865 | 0.253 | 2 | 24 | voltage-gated channel activity |
| GO: Molecular function | GO:0005267 | 0.02799 | 8.477 | 0.264 | 2 | 25 | potassium channel activity |
| GO: Molecular function | GO:0016788 | 0.02882 | 2.814 | 2.362 | 6 | 224 | hydrolase activity, acting on ester bonds |
| GO: Molecular function | GO:0034979 | 0.03131 | 47.913 | 0.032 | 1 | 3 | NAD-dependent protein deacetylase activity |
| GO: Molecular function | GO:0032041 | 0.03131 | 47.913 | 0.032 | 1 | 3 | NAD-dependent histone deacetylase activity (H3-K14 specific) |
| GO: Molecular function | GO:0004407 | 0.03131 | 47.913 | 0.032 | 1 | 3 | histone deacetylase activity |
| GO: Molecular function | GO:0000213 | 0.03131 | 47.913 | 0.032 | 1 | 3 | tRNA-intron endonuclease activity |
| GO: Molecular function | GO:0019213 | 0.04153 | 31.935 | 0.042 | 1 | 4 | deacetylase activity |
| GO: Molecular function | GO:0046912 | 0.04153 | 31.935 | 0.042 | 1 | 4 | transferase activity, transferring acyl groups, acyl groups converted into alkyl on transfer |
| GO: Molecular function | GO:0017150 | 0.04153 | 31.935 | 0.042 | 1 | 4 | tRNA dihydrouridine synthase activity |
| GO: Cellular component | GO:0005815 | 0.00842 | 17.054 | 0.142 | 2 | 15 | microtubule organizing center |
| GO: Cellular component | GO:0016514 | 0.00944 | Inf | 0.009 | 1 | 1 | SWI/SNF complex |
| GO: Cellular component | GO:0000118 | 0.00944 | Inf | 0.009 | 1 | 1 | histone deacetylase complex |
| GO: Cellular component | GO:0016012 | 0.02807 | 53.956 | 0.028 | 1 | 3 | sarcoglycan complex |
| GO: Cellular component | GO:0005761 | 0.04636 | 26.963 | 0.047 | 1 | 5 | mitochondrial ribosome |
Table S17: Results of KEGG and GO enrichment analysis on the list of genes that were significantly upregulated in the control group in L. flavus. The gene universe was defined as all L. flavus genes for which we detected an A. mellifera ortholog.
# The gene universe is all L. flavus genes for which we found a BLAST hit in Apis mellifera
gene.universe.flavus <- (left_join(tbl(my_db, "rsem_lf") %>%
dplyr::select(gene),
tbl(my_db, "lf2am") %>%
dplyr::rename(gene = lf), by = "gene") %>%
dplyr::select(am) %>%
filter(!is.na(am)) %>%
as.data.frame())[,1] %>% unique
# The test set is all differentially expressed genes in L. flavus for which we found a BLAST hit in Apis
up.in.control.flavus <- (flavus.de %>% filter(`Log2 FC` > 0 & `Apis BLAST` != " ") %>% as.data.frame())$`Apis BLAST` %>% unique
GO.and.KEGG.enrichment(up.in.control.flavus, gene.universe.flavus)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04142 | 0.01744 | 6.386 | 0.568 | 3 | 41 | Lysosome |
| GO: Biological process | GO:0042278 | 0.00412 | 11.415 | 0.340 | 3 | 30 | purine nucleoside metabolic process |
| GO: Biological process | GO:0015991 | 0.00519 | 24.375 | 0.113 | 2 | 10 | ATP hydrolysis coupled proton transport |
| GO: Biological process | GO:0009119 | 0.00750 | 9.024 | 0.420 | 3 | 37 | ribonucleoside metabolic process |
| GO: Biological process | GO:1901657 | 0.01000 | 8.053 | 0.465 | 3 | 41 | glycosyl compound metabolic process |
| GO: Biological process | GO:0006422 | 0.01135 | Inf | 0.011 | 1 | 1 | aspartyl-tRNA aminoacylation |
| GO: Biological process | GO:0006285 | 0.01135 | Inf | 0.011 | 1 | 1 | base-excision repair, AP site formation |
| GO: Biological process | GO:0003012 | 0.01135 | Inf | 0.011 | 1 | 1 | muscle system process |
| GO: Biological process | GO:0031032 | 0.01135 | Inf | 0.011 | 1 | 1 | actomyosin structure organization |
| GO: Biological process | GO:0006937 | 0.01135 | Inf | 0.011 | 1 | 1 | regulation of muscle contraction |
| GO: Biological process | GO:1902600 | 0.01171 | 14.952 | 0.170 | 2 | 15 | hydrogen ion transmembrane transport |
| GO: Biological process | GO:0098660 | 0.01171 | 14.952 | 0.170 | 2 | 15 | inorganic ion transmembrane transport |
| GO: Biological process | GO:0098655 | 0.01171 | 14.952 | 0.170 | 2 | 15 | cation transmembrane transport |
| GO: Biological process | GO:0006818 | 0.01329 | 13.875 | 0.182 | 2 | 16 | hydrogen transport |
| GO: Biological process | GO:0046034 | 0.01672 | 12.125 | 0.204 | 2 | 18 | ATP metabolic process |
| GO: Biological process | GO:0015672 | 0.01856 | 11.404 | 0.216 | 2 | 19 | monovalent inorganic cation transport |
| GO: Biological process | GO:0009144 | 0.02249 | 10.191 | 0.238 | 2 | 21 | purine nucleoside triphosphate metabolic process |
| GO: Biological process | GO:0044057 | 0.02258 | 92.176 | 0.023 | 1 | 2 | regulation of system process |
| GO: Biological process | GO:0000096 | 0.02258 | 92.176 | 0.023 | 1 | 2 | sulfur amino acid metabolic process |
| GO: Biological process | GO:0019284 | 0.02258 | 92.176 | 0.023 | 1 | 2 | L-methionine biosynthetic process from S-adenosylmethionine |
| GO: Biological process | GO:0046498 | 0.02258 | 92.176 | 0.023 | 1 | 2 | S-adenosylhomocysteine metabolic process |
| GO: Biological process | GO:0009199 | 0.02674 | 9.208 | 0.261 | 2 | 23 | ribonucleoside triphosphate metabolic process |
| GO: Biological process | GO:0009126 | 0.03366 | 8.042 | 0.295 | 2 | 26 | purine nucleoside monophosphate metabolic process |
| GO: Biological process | GO:0019509 | 0.03368 | 46.059 | 0.034 | 1 | 3 | L-methionine biosynthetic process from methylthioadenosine |
| GO: Biological process | GO:0071265 | 0.03368 | 46.059 | 0.034 | 1 | 3 | L-methionine biosynthetic process |
| GO: Biological process | GO:0043102 | 0.03368 | 46.059 | 0.034 | 1 | 3 | amino acid salvage |
| GO: Biological process | GO:0007205 | 0.03368 | 46.059 | 0.034 | 1 | 3 | protein kinase C-activating G-protein coupled receptor signaling pathway |
| GO: Biological process | GO:0055085 | 0.03452 | 4.858 | 0.738 | 3 | 65 | transmembrane transport |
| GO: Biological process | GO:0009161 | 0.04387 | 6.875 | 0.340 | 2 | 30 | ribonucleoside monophosphate metabolic process |
| GO: Biological process | GO:0009067 | 0.04467 | 30.686 | 0.045 | 1 | 4 | aspartate family amino acid biosynthetic process |
| GO: Biological process | GO:0042181 | 0.04467 | 30.686 | 0.045 | 1 | 4 | ketone biosynthetic process |
| GO: Biological process | GO:0006108 | 0.04467 | 30.686 | 0.045 | 1 | 4 | malate metabolic process |
| GO: Biological process | GO:0006744 | 0.04467 | 30.686 | 0.045 | 1 | 4 | ubiquinone biosynthetic process |
| GO: Biological process | GO:0006555 | 0.04467 | 30.686 | 0.045 | 1 | 4 | methionine metabolic process |
| GO: Biological process | GO:1901661 | 0.04467 | 30.686 | 0.045 | 1 | 4 | quinone metabolic process |
| GO: Biological process | GO:0055086 | 0.04484 | 4.345 | 0.817 | 3 | 72 | nucleobase-containing small molecule metabolic process |
| GO: Biological process | GO:0006163 | 0.04658 | 6.634 | 0.352 | 2 | 31 | purine nucleotide metabolic process |
| GO: Molecular function | GO:0044769 | 0.00552 | 23.648 | 0.117 | 2 | 8 | ATPase activity, coupled to transmembrane movement of ions, rotational mechanism |
| GO: Molecular function | GO:0008169 | 0.01463 | Inf | 0.015 | 1 | 1 | C-methyltransferase activity |
| GO: Molecular function | GO:0004054 | 0.01463 | Inf | 0.015 | 1 | 1 | arginine kinase activity |
| GO: Molecular function | GO:0019104 | 0.01463 | Inf | 0.015 | 1 | 1 | DNA N-glycosylase activity |
| GO: Molecular function | GO:0000703 | 0.01463 | Inf | 0.015 | 1 | 1 | oxidized pyrimidine nucleobase lesion DNA N-glycosylase activity |
| GO: Molecular function | GO:0004815 | 0.01463 | Inf | 0.015 | 1 | 1 | aspartate-tRNA ligase activity |
| GO: Molecular function | GO:0046570 | 0.01463 | Inf | 0.015 | 1 | 1 | methylthioribulose 1-phosphate dehydratase activity |
| GO: Molecular function | GO:0008425 | 0.01463 | Inf | 0.015 | 1 | 1 | 2-polyprenyl-6-methoxy-1,4-benzoquinone methyltransferase activity |
| GO: Molecular function | GO:0019829 | 0.01468 | 12.874 | 0.190 | 2 | 13 | cation-transporting ATPase activity |
| GO: Molecular function | GO:0016835 | 0.02197 | 10.103 | 0.234 | 2 | 16 | carbon-oxygen lyase activity |
| GO: Molecular function | GO:0022853 | 0.02468 | 9.426 | 0.249 | 2 | 17 | active ion transmembrane transporter activity |
| GO: Molecular function | GO:0046872 | 0.02757 | 2.074 | 8.425 | 14 | 576 | metal ion binding |
| GO: Molecular function | GO:0030151 | 0.02904 | 69.162 | 0.029 | 1 | 2 | molybdenum ion binding |
| GO: Molecular function | GO:0004471 | 0.02904 | 69.162 | 0.029 | 1 | 2 | malate dehydrogenase (decarboxylating) (NAD+) activity |
| GO: Molecular function | GO:0016972 | 0.02904 | 69.162 | 0.029 | 1 | 2 | thiol oxidase activity |
| GO: Molecular function | GO:0015078 | 0.03673 | 7.430 | 0.307 | 2 | 21 | hydrogen ion transmembrane transporter activity |
| GO: Molecular function | GO:0043167 | 0.03923 | 1.956 | 8.805 | 14 | 602 | ion binding |
| GO: Molecular function | GO:0004181 | 0.04326 | 34.568 | 0.044 | 1 | 3 | metallocarboxypeptidase activity |
| GO: Molecular function | GO:0004143 | 0.04326 | 34.568 | 0.044 | 1 | 3 | diacylglycerol kinase activity |
| GO: Molecular function | GO:0015399 | 0.04346 | 6.717 | 0.336 | 2 | 23 | primary active transmembrane transporter activity |
| GO: Molecular function | GO:0042626 | 0.04346 | 6.717 | 0.336 | 2 | 23 | ATPase activity, coupled to transmembrane movement of substances |
| GO: Molecular function | GO:0003824 | 0.04989 | 1.861 | 20.521 | 26 | 1403 | catalytic activity |
| GO: Cellular component | GO:0043292 | 0.00009 | Inf | 0.020 | 2 | 2 | contractile fiber |
| GO: Cellular component | GO:0005861 | 0.00009 | Inf | 0.020 | 2 | 2 | troponin complex |
| GO: Cellular component | GO:0036379 | 0.00009 | Inf | 0.020 | 2 | 2 | myofilament |
| GO: Cellular component | GO:0030017 | 0.00009 | Inf | 0.020 | 2 | 2 | sarcomere |
| GO: Cellular component | GO:0016469 | 0.00902 | 16.947 | 0.148 | 2 | 15 | proton-transporting two-sector ATPase complex |
| GO: Cellular component | GO:0042600 | 0.00987 | Inf | 0.010 | 1 | 1 | chorion |
| GO: Cellular component | GO:0005623 | 0.02283 | 2.921 | 11.028 | 16 | 1117 | cell |
| GO: Cellular component | GO:0015629 | 0.02430 | 9.533 | 0.247 | 2 | 25 | actin cytoskeleton |
| GO: Cellular component | GO:0033180 | 0.02934 | 52.600 | 0.030 | 1 | 3 | proton-transporting V-type ATPase, V1 domain |
| GO: Cellular component | GO:0045261 | 0.03894 | 35.050 | 0.039 | 1 | 4 | proton-transporting ATP synthase complex, catalytic core F(1) |
Table S18: Results of KEGG and GO enrichment analysis on the list of genes that were significantly upregulated in the queen pheromone treatment in L. flavus. The gene universe was defined as all L. flavus genes for which we detected an A. mellifera ortholog.
up.in.QP.flavus <- (flavus.de %>% filter(`Log2 FC` < 0 & `Apis BLAST` != " ") %>% as.data.frame())$`Apis BLAST` %>% unique
GO.and.KEGG.enrichment(up.in.QP.flavus, gene.universe.flavus)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04146 | 0.00009 | 10.553 | 0.798 | 6 | 39 | Peroxisome |
| KEGG | KEGG:04141 | 0.00089 | 5.557 | 1.657 | 7 | 81 | Protein processing in endoplasmic reticulum |
| KEGG | KEGG:01212 | 0.00157 | 9.845 | 0.532 | 4 | 26 | Fatty acid metabolism |
| KEGG | KEGG:00030 | 0.00243 | 14.347 | 0.286 | 3 | 14 | Pentose phosphate pathway |
| KEGG | KEGG:01200 | 0.00507 | 5.296 | 1.166 | 5 | 57 | Carbon metabolism |
| KEGG | KEGG:00071 | 0.00699 | 9.246 | 0.409 | 3 | 20 | Fatty acid degradation |
| KEGG | KEGG:01040 | 0.00799 | 20.400 | 0.143 | 2 | 7 | Biosynthesis of unsaturated fatty acids |
| KEGG | KEGG:00981 | 0.00799 | 20.400 | 0.143 | 2 | 7 | Insect hormone biosynthesis |
| KEGG | KEGG:00061 | 0.01051 | 16.989 | 0.164 | 2 | 8 | Fatty acid biosynthesis |
| KEGG | KEGG:00062 | 0.01987 | 11.303 | 0.225 | 2 | 11 | Fatty acid elongation |
| KEGG | KEGG:03050 | 0.02168 | 5.782 | 0.614 | 3 | 30 | Proteasome |
| KEGG | KEGG:00052 | 0.02355 | 10.166 | 0.246 | 2 | 12 | Galactose metabolism |
| KEGG | KEGG:01230 | 0.03262 | 4.862 | 0.716 | 3 | 35 | Biosynthesis of amino acids |
| KEGG | KEGG:00410 | 0.03606 | 7.804 | 0.307 | 2 | 15 | beta-Alanine metabolism |
| KEGG | KEGG:00380 | 0.03606 | 7.804 | 0.307 | 2 | 15 | Tryptophan metabolism |
| GO: Biological process | GO:0006098 | 0.00119 | 65.208 | 0.057 | 2 | 5 | pentose-phosphate shunt |
| GO: Biological process | GO:0006081 | 0.00119 | 65.208 | 0.057 | 2 | 5 | cellular aldehyde metabolic process |
| GO: Biological process | GO:0006629 | 0.00633 | 6.607 | 0.783 | 4 | 69 | lipid metabolic process |
| GO: Biological process | GO:0046496 | 0.01022 | 16.208 | 0.159 | 2 | 14 | nicotinamide nucleotide metabolic process |
| GO: Biological process | GO:0006102 | 0.01135 | Inf | 0.011 | 1 | 1 | isocitrate metabolic process |
| GO: Biological process | GO:0044242 | 0.01135 | Inf | 0.011 | 1 | 1 | cellular lipid catabolic process |
| GO: Biological process | GO:0015910 | 0.01135 | Inf | 0.011 | 1 | 1 | peroxisomal long-chain fatty acid import |
| GO: Biological process | GO:0015908 | 0.01135 | Inf | 0.011 | 1 | 1 | fatty acid transport |
| GO: Biological process | GO:0006635 | 0.01135 | Inf | 0.011 | 1 | 1 | fatty acid beta-oxidation |
| GO: Biological process | GO:0034440 | 0.01135 | Inf | 0.011 | 1 | 1 | lipid oxidation |
| GO: Biological process | GO:0072329 | 0.01135 | Inf | 0.011 | 1 | 1 | monocarboxylic acid catabolic process |
| GO: Biological process | GO:0072524 | 0.01171 | 14.952 | 0.170 | 2 | 15 | pyridine-containing compound metabolic process |
| GO: Biological process | GO:0006631 | 0.01329 | 13.875 | 0.182 | 2 | 16 | fatty acid metabolic process |
| GO: Biological process | GO:0006733 | 0.01672 | 12.125 | 0.204 | 2 | 18 | oxidoreduction coenzyme metabolic process |
| GO: Biological process | GO:0044281 | 0.01784 | 3.583 | 2.247 | 6 | 198 | small molecule metabolic process |
| GO: Biological process | GO:0005991 | 0.02258 | 92.176 | 0.023 | 1 | 2 | trehalose metabolic process |
| GO: Biological process | GO:0006012 | 0.03368 | 46.059 | 0.034 | 1 | 3 | galactose metabolic process |
| GO: Biological process | GO:0046942 | 0.03368 | 46.059 | 0.034 | 1 | 3 | carboxylic acid transport |
| GO: Biological process | GO:0009311 | 0.04467 | 30.686 | 0.045 | 1 | 4 | oligosaccharide metabolic process |
| GO: Biological process | GO:0006820 | 0.04467 | 30.686 | 0.045 | 1 | 4 | anion transport |
| GO: Biological process | GO:0005975 | 0.04484 | 4.345 | 0.817 | 3 | 72 | carbohydrate metabolic process |
| GO: Molecular function | GO:0016491 | 0.00459 | 3.556 | 2.730 | 8 | 184 | oxidoreductase activity |
| GO: Molecular function | GO:0033961 | 0.01578 | Inf | 0.016 | 1 | 1 | cis-stilbene-oxide hydrolase activity |
| GO: Molecular function | GO:0004801 | 0.01578 | Inf | 0.016 | 1 | 1 | sedoheptulose-7-phosphate:D-glyceraldehyde-3-phosphate glyceronetransferase activity |
| GO: Molecular function | GO:0004335 | 0.01578 | Inf | 0.016 | 1 | 1 | galactokinase activity |
| GO: Molecular function | GO:0004300 | 0.01578 | Inf | 0.016 | 1 | 1 | enoyl-CoA hydratase activity |
| GO: Molecular function | GO:0004450 | 0.01578 | Inf | 0.016 | 1 | 1 | isocitrate dehydrogenase (NADP+) activity |
| GO: Molecular function | GO:0016620 | 0.01698 | 11.869 | 0.205 | 2 | 13 | oxidoreductase activity, acting on the aldehyde or oxo group of donors, NAD or NADP as acceptor |
| GO: Molecular function | GO:0016614 | 0.01955 | 5.858 | 0.584 | 3 | 37 | oxidoreductase activity, acting on CH-OH group of donors |
| GO: Molecular function | GO:0004784 | 0.03132 | 63.900 | 0.032 | 1 | 2 | superoxide dismutase activity |
| GO: Molecular function | GO:0003756 | 0.03132 | 63.900 | 0.032 | 1 | 2 | protein disulfide isomerase activity |
| GO: Molecular function | GO:0004555 | 0.03132 | 63.900 | 0.032 | 1 | 2 | alpha,alpha-trehalase activity |
| GO: Molecular function | GO:0031177 | 0.03132 | 63.900 | 0.032 | 1 | 2 | phosphopantetheine binding |
| GO: Molecular function | GO:0003857 | 0.03132 | 63.900 | 0.032 | 1 | 2 | 3-hydroxyacyl-CoA dehydrogenase activity |
| GO: Molecular function | GO:0004185 | 0.03132 | 63.900 | 0.032 | 1 | 2 | serine-type carboxypeptidase activity |
| GO: Molecular function | GO:0016787 | 0.03223 | 2.005 | 8.555 | 14 | 555 | hydrolase activity |
| GO: Molecular function | GO:0016801 | 0.04662 | 31.938 | 0.047 | 1 | 3 | hydrolase activity, acting on ether bonds |
| GO: Molecular function | GO:0004616 | 0.04662 | 31.938 | 0.047 | 1 | 3 | phosphogluconate dehydrogenase (decarboxylating) activity |
| GO: Cellular component | GO:0005737 | 0.00040 | 4.662 | 4.444 | 12 | 411 | cytoplasm |
| GO: Cellular component | GO:0016507 | 0.01081 | Inf | 0.011 | 1 | 1 | mitochondrial fatty acid beta-oxidation multienzyme complex |
| GO: Cellular component | GO:0017119 | 0.03211 | 47.773 | 0.032 | 1 | 3 | Golgi transport complex |
| GO: Cellular component | GO:0005783 | 0.04558 | 6.584 | 0.346 | 2 | 32 | endoplasmic reticulum |
Table S19: Results of KEGG and GO enrichment analysis on the list of genes that were significantly upregulated in the control group in L. niger The gene universe was defined as all L. niger genes for which we detected an A. mellifera ortholog.
# The gene universe is all L. flavus genes for which we found a BLAST hit in Apis mellifera
gene.universe.niger <- (left_join(tbl(my_db, "rsem_ln") %>%
dplyr::select(gene),
tbl(my_db, "ln2am") %>%
dplyr::rename(gene = ln), by = "gene") %>%
dplyr::select(am) %>%
filter(!is.na(am)) %>%
as.data.frame())[,1] %>% unique
# The test set is all differentially expressed genes in L. flavus for which we found a BLAST hit in Apis
up.in.control.niger <- (niger.de %>% filter(`Log2 FC` > 0 & `Apis BLAST` != " ") %>% as.data.frame())$`Apis BLAST` %>% unique
GO.and.KEGG.enrichment(up.in.control.niger, gene.universe.niger)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04145 | 0.00336 | 12.834 | 0.322 | 3 | 35 | Phagosome |
| KEGG | KEGG:01230 | 0.00426 | 11.709 | 0.349 | 3 | 38 | Biosynthesis of amino acids |
| KEGG | KEGG:04745 | 0.00489 | 25.291 | 0.110 | 2 | 12 | Phototransduction - fly |
| KEGG | KEGG:01100 | 0.00511 | 5.064 | 4.045 | 9 | 440 | Metabolic pathways |
| KEGG | KEGG:00030 | 0.00575 | 22.975 | 0.120 | 2 | 13 | Pentose phosphate pathway |
| KEGG | KEGG:00330 | 0.00575 | 22.975 | 0.120 | 2 | 13 | Arginine and proline metabolism |
| KEGG | KEGG:04391 | 0.02240 | 10.432 | 0.239 | 2 | 26 | Hippo signaling pathway - fly |
| KEGG | KEGG:00920 | 0.02735 | 58.292 | 0.028 | 1 | 3 | Sulfur metabolism |
| KEGG | KEGG:00603 | 0.04519 | 29.104 | 0.046 | 1 | 5 | Glycosphingolipid biosynthesis - globo series |
| KEGG | KEGG:00130 | 0.04519 | 29.104 | 0.046 | 1 | 5 | Ubiquinone and other terpenoid-quinone biosynthesis |
| GO: Biological process | GO:0006753 | 0.00096 | 12.285 | 0.484 | 4 | 57 | nucleoside phosphate metabolic process |
| GO: Biological process | GO:0009126 | 0.00099 | 20.400 | 0.212 | 3 | 25 | purine nucleoside monophosphate metabolic process |
| GO: Biological process | GO:0006163 | 0.00154 | 17.215 | 0.246 | 3 | 29 | purine nucleotide metabolic process |
| GO: Biological process | GO:0042278 | 0.00154 | 17.215 | 0.246 | 3 | 29 | purine nucleoside metabolic process |
| GO: Biological process | GO:0009161 | 0.00154 | 17.215 | 0.246 | 3 | 29 | ribonucleoside monophosphate metabolic process |
| GO: Biological process | GO:0044281 | 0.00158 | 7.319 | 1.478 | 6 | 188 | small molecule metabolic process |
| GO: Biological process | GO:0009259 | 0.00225 | 14.880 | 0.280 | 3 | 33 | ribonucleotide metabolic process |
| GO: Biological process | GO:0009119 | 0.00268 | 13.931 | 0.297 | 3 | 35 | ribonucleoside metabolic process |
| GO: Biological process | GO:1901657 | 0.00340 | 12.711 | 0.323 | 3 | 38 | glycosyl compound metabolic process |
| GO: Biological process | GO:0019362 | 0.00493 | 24.909 | 0.110 | 2 | 13 | pyridine nucleotide metabolic process |
| GO: Biological process | GO:0009168 | 0.00747 | 19.532 | 0.136 | 2 | 16 | purine ribonucleoside monophosphate biosynthetic process |
| GO: Biological process | GO:0006793 | 0.00803 | 6.511 | 0.858 | 4 | 101 | phosphorus metabolic process |
| GO: Biological process | GO:0046034 | 0.00843 | 18.218 | 0.144 | 2 | 17 | ATP metabolic process |
| GO: Biological process | GO:0031032 | 0.00849 | Inf | 0.008 | 1 | 1 | actomyosin structure organization |
| GO: Biological process | GO:0046129 | 0.00944 | 17.068 | 0.153 | 2 | 18 | purine ribonucleoside biosynthetic process |
| GO: Biological process | GO:0009152 | 0.01050 | 16.053 | 0.161 | 2 | 19 | purine ribonucleotide biosynthetic process |
| GO: Biological process | GO:0009144 | 0.01161 | 15.152 | 0.170 | 2 | 20 | purine nucleoside triphosphate metabolic process |
| GO: Biological process | GO:0009124 | 0.01277 | 14.344 | 0.178 | 2 | 21 | nucleoside monophosphate biosynthetic process |
| GO: Biological process | GO:0009199 | 0.01398 | 13.618 | 0.187 | 2 | 22 | ribonucleoside triphosphate metabolic process |
| GO: Biological process | GO:0072522 | 0.01523 | 12.961 | 0.195 | 2 | 23 | purine-containing compound biosynthetic process |
| GO: Biological process | GO:0044699 | 0.01590 | 4.333 | 5.689 | 10 | 670 | single-organism process |
| GO: Biological process | GO:0009163 | 0.01654 | 12.364 | 0.204 | 2 | 24 | nucleoside biosynthetic process |
| GO: Biological process | GO:0046390 | 0.01654 | 12.364 | 0.204 | 2 | 24 | ribose phosphate biosynthetic process |
| GO: Biological process | GO:0044208 | 0.01692 | 126.417 | 0.017 | 1 | 2 | ‘de novo’ AMP biosynthetic process |
| GO: Biological process | GO:0055129 | 0.01692 | 126.417 | 0.017 | 1 | 2 | L-proline biosynthetic process |
| GO: Biological process | GO:0006165 | 0.02527 | 63.167 | 0.025 | 1 | 3 | nucleoside diphosphate phosphorylation |
| GO: Biological process | GO:0006560 | 0.02527 | 63.167 | 0.025 | 1 | 3 | proline metabolic process |
| GO: Biological process | GO:0006096 | 0.02527 | 63.167 | 0.025 | 1 | 3 | glycolytic process |
| GO: Biological process | GO:0006189 | 0.03357 | 42.083 | 0.034 | 1 | 4 | ‘de novo’ IMP biosynthetic process |
| GO: Biological process | GO:0046040 | 0.03357 | 42.083 | 0.034 | 1 | 4 | IMP metabolic process |
| GO: Biological process | GO:0046033 | 0.03357 | 42.083 | 0.034 | 1 | 4 | AMP metabolic process |
| GO: Biological process | GO:0006732 | 0.03382 | 8.182 | 0.297 | 2 | 35 | coenzyme metabolic process |
| GO: Biological process | GO:1901564 | 0.03621 | 3.609 | 2.007 | 5 | 255 | organonitrogen compound metabolic process |
| GO: Biological process | GO:0009165 | 0.03750 | 7.704 | 0.314 | 2 | 37 | nucleotide biosynthetic process |
| GO: Biological process | GO:0009084 | 0.04179 | 31.542 | 0.042 | 1 | 5 | glutamine family amino acid biosynthetic process |
| GO: Biological process | GO:0006730 | 0.04179 | 31.542 | 0.042 | 1 | 5 | one-carbon metabolic process |
| GO: Biological process | GO:0009185 | 0.04179 | 31.542 | 0.042 | 1 | 5 | ribonucleoside diphosphate metabolic process |
| GO: Biological process | GO:0009135 | 0.04179 | 31.542 | 0.042 | 1 | 5 | purine nucleoside diphosphate metabolic process |
| GO: Biological process | GO:0006098 | 0.04179 | 31.542 | 0.042 | 1 | 5 | pentose-phosphate shunt |
| GO: Biological process | GO:0046031 | 0.04179 | 31.542 | 0.042 | 1 | 5 | ADP metabolic process |
| GO: Biological process | GO:0006081 | 0.04179 | 31.542 | 0.042 | 1 | 5 | cellular aldehyde metabolic process |
| GO: Biological process | GO:0016052 | 0.04179 | 31.542 | 0.042 | 1 | 5 | carbohydrate catabolic process |
| GO: Biological process | GO:0009072 | 0.04996 | 25.217 | 0.051 | 1 | 6 | aromatic amino acid family metabolic process |
| GO: Biological process | GO:0006979 | 0.04996 | 25.217 | 0.051 | 1 | 6 | response to oxidative stress |
| GO: Molecular function | GO:0020037 | 0.00007 | 24.157 | 0.234 | 4 | 28 | heme binding |
| GO: Molecular function | GO:0004054 | 0.00837 | Inf | 0.008 | 1 | 1 | arginine kinase activity |
| GO: Molecular function | GO:0004018 | 0.00837 | Inf | 0.008 | 1 | 1 | N6-(1,2-dicarboxyethyl)AMP AMP-lyase (fumarate-forming) activity |
| GO: Molecular function | GO:0016840 | 0.00837 | Inf | 0.008 | 1 | 1 | carbon-nitrogen lyase activity |
| GO: Molecular function | GO:0004801 | 0.00837 | Inf | 0.008 | 1 | 1 | sedoheptulose-7-phosphate:D-glyceraldehyde-3-phosphate glyceronetransferase activity |
| GO: Molecular function | GO:0004332 | 0.00837 | Inf | 0.008 | 1 | 1 | fructose-bisphosphate aldolase activity |
| GO: Molecular function | GO:0070626 | 0.00837 | Inf | 0.008 | 1 | 1 | (S)-2-(5-amino-1-(5-phospho-D-ribosyl)imidazole-4-carboxamido)succinate AMP-lyase (fumarate-forming) activity |
| GO: Molecular function | GO:0003868 | 0.00837 | Inf | 0.008 | 1 | 1 | 4-hydroxyphenylpyruvate dioxygenase activity |
| GO: Molecular function | GO:0004013 | 0.01667 | 124.350 | 0.017 | 1 | 2 | adenosylhomocysteinase activity |
| GO: Molecular function | GO:0004735 | 0.01667 | 124.350 | 0.017 | 1 | 2 | pyrroline-5-carboxylate reductase activity |
| GO: Molecular function | GO:0004497 | 0.01922 | 10.807 | 0.218 | 2 | 26 | monooxygenase activity |
| GO: Molecular function | GO:0016701 | 0.02491 | 62.150 | 0.025 | 1 | 3 | oxidoreductase activity, acting on single donors with incorporation of molecular oxygen |
| GO: Molecular function | GO:0016801 | 0.02491 | 62.150 | 0.025 | 1 | 3 | hydrolase activity, acting on ether bonds |
| GO: Molecular function | GO:0005506 | 0.02521 | 9.248 | 0.251 | 2 | 30 | iron ion binding |
| GO: Molecular function | GO:0016705 | 0.03015 | 8.343 | 0.276 | 2 | 33 | oxidoreductase activity, acting on paired donors, with incorporation or reduction of molecular oxygen |
| GO: Molecular function | GO:0051213 | 0.03308 | 41.417 | 0.033 | 1 | 4 | dioxygenase activity |
| GO: Molecular function | GO:0004601 | 0.03308 | 41.417 | 0.033 | 1 | 4 | peroxidase activity |
| GO: Molecular function | GO:0046933 | 0.04923 | 24.830 | 0.050 | 1 | 6 | proton-transporting ATP synthase activity, rotational mechanism |
| GO: Molecular function | GO:0016645 | 0.04923 | 24.830 | 0.050 | 1 | 6 | oxidoreductase activity, acting on the CH-NH group of donors |
| GO: Cellular component | GO:0005856 | 0.00494 | 11.488 | 0.373 | 3 | 75 | cytoskeleton |
| GO: Cellular component | GO:0042600 | 0.00497 | Inf | 0.005 | 1 | 1 | chorion |
| GO: Cellular component | GO:0043292 | 0.00497 | Inf | 0.005 | 1 | 1 | contractile fiber |
| GO: Cellular component | GO:0005861 | 0.00497 | Inf | 0.005 | 1 | 1 | troponin complex |
| GO: Cellular component | GO:0036379 | 0.00497 | Inf | 0.005 | 1 | 1 | myofilament |
| GO: Cellular component | GO:0030017 | 0.00497 | Inf | 0.005 | 1 | 1 | sarcomere |
| GO: Cellular component | GO:0044422 | 0.00666 | 6.360 | 1.377 | 5 | 277 | organelle part |
| GO: Cellular component | GO:0005758 | 0.01484 | 111.111 | 0.015 | 1 | 3 | mitochondrial intermembrane space |
| GO: Cellular component | GO:0031967 | 0.01568 | 12.921 | 0.199 | 2 | 40 | organelle envelope |
| GO: Cellular component | GO:0045261 | 0.01975 | 74.037 | 0.020 | 1 | 4 | proton-transporting ATP synthase complex, catalytic core F(1) |
| GO: Cellular component | GO:0005737 | 0.02916 | 4.173 | 1.948 | 5 | 392 | cytoplasm |
| GO: Cellular component | GO:0070469 | 0.03433 | 36.963 | 0.035 | 1 | 7 | respiratory chain |
| GO: Cellular component | GO:0005739 | 0.03479 | 8.233 | 0.303 | 2 | 61 | mitochondrion |
| GO: Cellular component | GO:0016459 | 0.04871 | 24.605 | 0.050 | 1 | 10 | myosin complex |
Table S20: Results of KEGG and GO enrichment analysis on the list of genes that were significantly upregulated in the queen pheromone treatment in L. niger The gene universe was defined as all L. niger genes for which we detected an A. mellifera ortholog.
up.in.QP.niger <- (niger.de %>% filter(`Log2 FC` < 0 & `Apis BLAST` != " ") %>% as.data.frame())$`Apis BLAST` %>% unique
GO.and.KEGG.enrichment(up.in.QP.niger, gene.universe.niger)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:01200 | 0.00004 | 13.186 | 0.726 | 6 | 57 | Carbon metabolism |
| KEGG | KEGG:01212 | 0.00230 | 14.495 | 0.280 | 3 | 22 | Fatty acid metabolism |
| KEGG | KEGG:00061 | 0.00410 | 28.958 | 0.102 | 2 | 8 | Fatty acid biosynthesis |
| KEGG | KEGG:04146 | 0.00682 | 9.428 | 0.407 | 3 | 32 | Peroxisome |
| KEGG | KEGG:01100 | 0.00788 | 3.542 | 5.601 | 11 | 440 | Metabolic pathways |
| KEGG | KEGG:00030 | 0.01099 | 15.739 | 0.165 | 2 | 13 | Pentose phosphate pathway |
| KEGG | KEGG:00640 | 0.01860 | 11.508 | 0.216 | 2 | 17 | Propanoate metabolism |
| KEGG | KEGG:00620 | 0.02540 | 9.569 | 0.255 | 2 | 20 | Pyruvate metabolism |
| GO: Biological process | GO:0006733 | 0.00496 | 25.100 | 0.111 | 2 | 17 | oxidoreduction coenzyme metabolic process |
| GO: Biological process | GO:0042744 | 0.00653 | Inf | 0.007 | 1 | 1 | hydrogen peroxide catabolic process |
| GO: Biological process | GO:0072593 | 0.00653 | Inf | 0.007 | 1 | 1 | reactive oxygen species metabolic process |
| GO: Biological process | GO:0042181 | 0.02590 | 56.222 | 0.026 | 1 | 4 | ketone biosynthetic process |
| GO: Biological process | GO:0006108 | 0.02590 | 56.222 | 0.026 | 1 | 4 | malate metabolic process |
| GO: Biological process | GO:0042773 | 0.02590 | 56.222 | 0.026 | 1 | 4 | ATP synthesis coupled electron transport |
| GO: Biological process | GO:0006744 | 0.02590 | 56.222 | 0.026 | 1 | 4 | ubiquinone biosynthetic process |
| GO: Biological process | GO:1901661 | 0.02590 | 56.222 | 0.026 | 1 | 4 | quinone metabolic process |
| GO: Biological process | GO:0044281 | 0.02780 | 4.698 | 1.261 | 4 | 193 | small molecule metabolic process |
| GO: Biological process | GO:0006098 | 0.03228 | 42.139 | 0.033 | 1 | 5 | pentose-phosphate shunt |
| GO: Biological process | GO:0006081 | 0.03228 | 42.139 | 0.033 | 1 | 5 | cellular aldehyde metabolic process |
| GO: Biological process | GO:0006979 | 0.03862 | 33.689 | 0.039 | 1 | 6 | response to oxidative stress |
| GO: Biological process | GO:0008152 | 0.04294 | 6.176 | 5.950 | 9 | 911 | metabolic process |
| GO: Biological process | GO:0009117 | 0.04899 | 6.792 | 0.366 | 2 | 56 | nucleotide metabolic process |
| GO: Molecular function | GO:0031177 | 0.00007 | Inf | 0.018 | 2 | 2 | phosphopantetheine binding |
| GO: Molecular function | GO:0016491 | 0.00013 | 10.633 | 0.889 | 6 | 135 | oxidoreductase activity |
| GO: Molecular function | GO:0020037 | 0.00166 | 15.549 | 0.246 | 3 | 28 | heme binding |
| GO: Molecular function | GO:0016627 | 0.00459 | 24.770 | 0.105 | 2 | 12 | oxidoreductase activity, acting on the CH-CH group of donors |
| GO: Molecular function | GO:0004096 | 0.00877 | Inf | 0.009 | 1 | 1 | catalase activity |
| GO: Molecular function | GO:0008169 | 0.00877 | Inf | 0.009 | 1 | 1 | C-methyltransferase activity |
| GO: Molecular function | GO:0016420 | 0.00877 | Inf | 0.009 | 1 | 1 | malonyltransferase activity |
| GO: Molecular function | GO:0004320 | 0.00877 | Inf | 0.009 | 1 | 1 | oleoyl-[acyl-carrier-protein] hydrolase activity |
| GO: Molecular function | GO:0004313 | 0.00877 | Inf | 0.009 | 1 | 1 | [acyl-carrier-protein] S-acetyltransferase activity |
| GO: Molecular function | GO:0004314 | 0.00877 | Inf | 0.009 | 1 | 1 | [acyl-carrier-protein] S-malonyltransferase activity |
| GO: Molecular function | GO:0004315 | 0.00877 | Inf | 0.009 | 1 | 1 | 3-oxoacyl-[acyl-carrier-protein] synthase activity |
| GO: Molecular function | GO:0004316 | 0.00877 | Inf | 0.009 | 1 | 1 | 3-oxoacyl-[acyl-carrier-protein] reductase (NADPH) activity |
| GO: Molecular function | GO:0004317 | 0.00877 | Inf | 0.009 | 1 | 1 | 3-hydroxypalmitoyl-[acyl-carrier-protein] dehydratase activity |
| GO: Molecular function | GO:0004319 | 0.00877 | Inf | 0.009 | 1 | 1 | enoyl-[acyl-carrier-protein] reductase (NADPH, B-specific) activity |
| GO: Molecular function | GO:0016295 | 0.00877 | Inf | 0.009 | 1 | 1 | myristoyl-[acyl-carrier-protein] hydrolase activity |
| GO: Molecular function | GO:0016296 | 0.00877 | Inf | 0.009 | 1 | 1 | palmitoyl-[acyl-carrier-protein] hydrolase activity |
| GO: Molecular function | GO:0016790 | 0.00877 | Inf | 0.009 | 1 | 1 | thiolester hydrolase activity |
| GO: Molecular function | GO:0008425 | 0.00877 | Inf | 0.009 | 1 | 1 | 2-polyprenyl-6-methoxy-1,4-benzoquinone methyltransferase activity |
| GO: Molecular function | GO:0004784 | 0.01746 | 118.381 | 0.018 | 1 | 2 | superoxide dismutase activity |
| GO: Molecular function | GO:0004471 | 0.01746 | 118.381 | 0.018 | 1 | 2 | malate dehydrogenase (decarboxylating) (NAD+) activity |
| GO: Molecular function | GO:0004616 | 0.01746 | 118.381 | 0.018 | 1 | 2 | phosphogluconate dehydrogenase (decarboxylating) activity |
| GO: Molecular function | GO:0004497 | 0.02101 | 10.262 | 0.228 | 2 | 26 | monooxygenase activity |
| GO: Molecular function | GO:0016614 | 0.02529 | 9.233 | 0.251 | 2 | 30 | oxidoreductase activity, acting on CH-OH group of donors |
| GO: Molecular function | GO:0005506 | 0.02753 | 8.782 | 0.263 | 2 | 30 | iron ion binding |
| GO: Molecular function | GO:0016705 | 0.03289 | 7.923 | 0.289 | 2 | 33 | oxidoreductase activity, acting on paired donors, with incorporation or reduction of molecular oxygen |
| GO: Molecular function | GO:0016615 | 0.03464 | 39.429 | 0.035 | 1 | 4 | malate dehydrogenase activity |
| GO: Molecular function | GO:0080019 | 0.04311 | 29.560 | 0.044 | 1 | 5 | fatty-acyl-CoA reductase (alcohol-forming) activity |
| GO: Cellular component | GO:0016021 | 0.03529 | 4.574 | 4.682 | 8 | 942 | integral component of membrane |
| GO: Cellular component | GO:0044425 | 0.04732 | 4.197 | 4.896 | 8 | 985 | membrane part |
Table S21: Results of KEGG and GO enrichment analysis on the list of genes showing significant differential expression in response to queen pheromone in two or more species. The gene universe was defined as all genes for which we found an ortholog in all four species.
overlap.gene.universe <- make.OGGs(c("am", "lf", "ln"))[[2]]$am # The gene universe is all genes that have orthologs in the 3 species that we tested for overlap
suppressWarnings(GO.and.KEGG.enrichment(all.overlaps, overlap.gene.universe))
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:01200 | 0.00006 | 18.047 | 0.484 | 5 | 45 | Carbon metabolism |
| KEGG | KEGG:00030 | 0.00020 | 39.533 | 0.129 | 3 | 12 | Pentose phosphate pathway |
| KEGG | KEGG:01212 | 0.02001 | 11.254 | 0.226 | 2 | 21 | Fatty acid metabolism |
| KEGG | KEGG:01100 | 0.02015 | 3.682 | 3.982 | 8 | 370 | Metabolic pathways |
| KEGG | KEGG:01230 | 0.04170 | 7.310 | 0.334 | 2 | 31 | Biosynthesis of amino acids |
| KEGG | KEGG:00130 | 0.04241 | 33.111 | 0.043 | 1 | 4 | Ubiquinone and other terpenoid-quinone biosynthesis |
| GO: Biological process | GO:0006733 | 0.00035 | 32.009 | 0.153 | 3 | 17 | oxidoreduction coenzyme metabolic process |
| GO: Biological process | GO:0006098 | 0.00073 | 89.333 | 0.045 | 2 | 5 | pentose-phosphate shunt |
| GO: Biological process | GO:0006081 | 0.00073 | 89.333 | 0.045 | 2 | 5 | cellular aldehyde metabolic process |
| GO: Biological process | GO:0072524 | 0.00546 | 24.202 | 0.117 | 2 | 13 | pyridine-containing compound metabolic process |
| GO: Biological process | GO:0046496 | 0.00546 | 24.202 | 0.117 | 2 | 13 | nicotinamide nucleotide metabolic process |
| GO: Biological process | GO:0031032 | 0.00902 | Inf | 0.009 | 1 | 1 | actomyosin structure organization |
| GO: Biological process | GO:0051186 | 0.03134 | 8.886 | 0.288 | 2 | 35 | cofactor metabolic process |
| GO: Biological process | GO:0042181 | 0.03562 | 40.200 | 0.036 | 1 | 4 | ketone biosynthetic process |
| GO: Biological process | GO:0006108 | 0.03562 | 40.200 | 0.036 | 1 | 4 | malate metabolic process |
| GO: Biological process | GO:0006744 | 0.03562 | 40.200 | 0.036 | 1 | 4 | ubiquinone biosynthetic process |
| GO: Biological process | GO:1901661 | 0.03562 | 40.200 | 0.036 | 1 | 4 | quinone metabolic process |
| GO: Biological process | GO:0006979 | 0.03562 | 40.200 | 0.036 | 1 | 4 | response to oxidative stress |
| GO: Biological process | GO:0044281 | 0.04119 | 3.974 | 1.407 | 4 | 156 | small molecule metabolic process |
| GO: Molecular function | GO:0016491 | 0.00095 | 5.808 | 1.721 | 7 | 161 | oxidoreductase activity |
| GO: Molecular function | GO:0020037 | 0.00917 | 16.939 | 0.150 | 2 | 14 | heme binding |
| GO: Molecular function | GO:0008169 | 0.01069 | Inf | 0.011 | 1 | 1 | C-methyltransferase activity |
| GO: Molecular function | GO:0004054 | 0.01069 | Inf | 0.011 | 1 | 1 | arginine kinase activity |
| GO: Molecular function | GO:0004801 | 0.01069 | Inf | 0.011 | 1 | 1 | sedoheptulose-7-phosphate:D-glyceraldehyde-3-phosphate glyceronetransferase activity |
| GO: Molecular function | GO:0008425 | 0.01069 | Inf | 0.011 | 1 | 1 | 2-polyprenyl-6-methoxy-1,4-benzoquinone methyltransferase activity |
| GO: Molecular function | GO:0004784 | 0.02128 | 97.100 | 0.021 | 1 | 2 | superoxide dismutase activity |
| GO: Molecular function | GO:0031177 | 0.02128 | 97.100 | 0.021 | 1 | 2 | phosphopantetheine binding |
| GO: Molecular function | GO:0004471 | 0.02128 | 97.100 | 0.021 | 1 | 2 | malate dehydrogenase (decarboxylating) (NAD+) activity |
| GO: Molecular function | GO:0004616 | 0.02128 | 97.100 | 0.021 | 1 | 2 | phosphogluconate dehydrogenase (decarboxylating) activity |
| GO: Molecular function | GO:0016615 | 0.04212 | 32.333 | 0.043 | 1 | 4 | malate dehydrogenase activity |
| GO: Molecular function | GO:0004601 | 0.04212 | 32.333 | 0.043 | 1 | 4 | peroxidase activity |
| GO: Cellular component | GO:0042600 | 0.00457 | Inf | 0.005 | 1 | 1 | chorion |
| GO: Cellular component | GO:0005737 | 0.03792 | 5.122 | 1.458 | 4 | 319 | cytoplasm |
| GO: Cellular component | GO:0005839 | 0.04048 | 31.604 | 0.041 | 1 | 9 | proteasome core complex |
# The gene universe is defined as all genes that have 2 or more isoforms. It would be anti-conservative if we instead included all genes, not just that are alternatively spliced
gene.universe.apis.splicing <- (tbl(my_db, "isoforms_am") %>%
group_by(gene) %>%
summarise(nIsoforms = n()) %>% filter(nIsoforms > 1) %>%
as.data.frame() %>%
dplyr::select(gene) %>% as.data.frame())[,1]
Table S22: Results of KEGG and GO enrichment analysis on the list of genes showing significant alternative splicing in A. mellifera. The gene universe was defined as all genes that showed alternative splicing in A. mellifera.
GO.and.KEGG.enrichment(am.alt.splice$Gene, gene.universe.apis.splicing)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04745 | 0.00580 | 24.049 | 0.122 | 2 | 11 | Phototransduction - fly |
| KEGG | KEGG:00564 | 0.04346 | 7.310 | 0.343 | 2 | 31 | Glycerophospholipid metabolism |
| GO: Biological process | GO:0007568 | 0.01189 | Inf | 0.012 | 1 | 1 | aging |
| GO: Biological process | GO:0032793 | 0.01189 | Inf | 0.012 | 1 | 1 | positive regulation of CREB transcription factor activity |
| GO: Biological process | GO:0090399 | 0.01189 | Inf | 0.012 | 1 | 1 | replicative senescence |
| GO: Biological process | GO:1901700 | 0.01189 | Inf | 0.012 | 1 | 1 | response to oxygen-containing compound |
| GO: Biological process | GO:0000723 | 0.01189 | Inf | 0.012 | 1 | 1 | telomere maintenance |
| GO: Biological process | GO:0010212 | 0.01189 | Inf | 0.012 | 1 | 1 | response to ionizing radiation |
| GO: Biological process | GO:0016572 | 0.01189 | Inf | 0.012 | 1 | 1 | histone phosphorylation |
| GO: Biological process | GO:1901031 | 0.01189 | Inf | 0.012 | 1 | 1 | regulation of response to reactive oxygen species |
| GO: Biological process | GO:0046470 | 0.01189 | Inf | 0.012 | 1 | 1 | phosphatidylcholine metabolic process |
| GO: Biological process | GO:0051103 | 0.02366 | 89.385 | 0.024 | 1 | 2 | DNA ligation involved in DNA repair |
| GO: Biological process | GO:0051090 | 0.02366 | 89.385 | 0.024 | 1 | 2 | regulation of sequence-specific DNA binding transcription factor activity |
| GO: Biological process | GO:0071897 | 0.02366 | 89.385 | 0.024 | 1 | 2 | DNA biosynthetic process |
| GO: Biological process | GO:0000075 | 0.02366 | 89.385 | 0.024 | 1 | 2 | cell cycle checkpoint |
| GO: Biological process | GO:0000077 | 0.02366 | 89.385 | 0.024 | 1 | 2 | DNA damage checkpoint |
| GO: Biological process | GO:0007049 | 0.03124 | 8.644 | 0.285 | 2 | 24 | cell cycle |
| GO: Biological process | GO:0007050 | 0.03529 | 44.654 | 0.036 | 1 | 3 | cell cycle arrest |
| GO: Biological process | GO:0080134 | 0.03529 | 44.654 | 0.036 | 1 | 3 | regulation of response to stress |
| GO: Biological process | GO:0033554 | 0.04442 | 7.012 | 0.345 | 2 | 29 | cellular response to stress |
| GO: Biological process | GO:0009628 | 0.04680 | 29.744 | 0.048 | 1 | 4 | response to abiotic stimulus |
| GO: Biological process | GO:0016569 | 0.04680 | 29.744 | 0.048 | 1 | 4 | chromatin modification |
| GO: Biological process | GO:0044093 | 0.04680 | 29.744 | 0.048 | 1 | 4 | positive regulation of molecular function |
| GO: Molecular function | GO:0001883 | 0.00254 | 3.828 | 3.916 | 10 | 355 | purine nucleoside binding |
| GO: Molecular function | GO:0032555 | 0.00254 | 3.828 | 3.916 | 10 | 355 | purine ribonucleotide binding |
| GO: Molecular function | GO:0032549 | 0.00260 | 3.815 | 3.927 | 10 | 356 | ribonucleoside binding |
| GO: Molecular function | GO:0005524 | 0.00299 | 3.912 | 3.309 | 9 | 300 | ATP binding |
| GO: Molecular function | GO:0030554 | 0.00306 | 3.897 | 3.320 | 9 | 301 | adenyl nucleotide binding |
| GO: Molecular function | GO:0097367 | 0.00421 | 3.529 | 4.181 | 10 | 379 | carbohydrate derivative binding |
| GO: Molecular function | GO:0000166 | 0.00670 | 3.175 | 5.218 | 11 | 473 | nucleotide binding |
| GO: Molecular function | GO:0004672 | 0.00971 | 4.535 | 1.368 | 5 | 124 | protein kinase activity |
| GO: Molecular function | GO:0005219 | 0.01103 | Inf | 0.011 | 1 | 1 | ryanodine-sensitive calcium-release channel activity |
| GO: Molecular function | GO:0060072 | 0.01103 | Inf | 0.011 | 1 | 1 | large conductance calcium-activated potassium channel activity |
| GO: Molecular function | GO:0004683 | 0.01103 | Inf | 0.011 | 1 | 1 | calmodulin-dependent protein kinase activity |
| GO: Molecular function | GO:0004622 | 0.01103 | Inf | 0.011 | 1 | 1 | lysophospholipase activity |
| GO: Molecular function | GO:0016772 | 0.01394 | 3.624 | 2.085 | 6 | 189 | transferase activity, transferring phosphorus-containing groups |
| GO: Molecular function | GO:0042626 | 0.02153 | 10.241 | 0.232 | 2 | 21 | ATPase activity, coupled to transmembrane movement of substances |
| GO: Molecular function | GO:0005227 | 0.02195 | 93.682 | 0.022 | 1 | 2 | calcium activated cation channel activity |
| GO: Molecular function | GO:0005217 | 0.02195 | 93.682 | 0.022 | 1 | 2 | intracellular ligand-gated ion channel activity |
| GO: Molecular function | GO:0099604 | 0.02195 | 93.682 | 0.022 | 1 | 2 | ligand-gated calcium channel activity |
| GO: Molecular function | GO:0003910 | 0.02195 | 93.682 | 0.022 | 1 | 2 | DNA ligase (ATP) activity |
| GO: Molecular function | GO:0015399 | 0.02352 | 9.724 | 0.243 | 2 | 22 | primary active transmembrane transporter activity |
| GO: Molecular function | GO:1901363 | 0.02650 | 2.469 | 8.946 | 14 | 811 | heterocyclic compound binding |
| GO: Molecular function | GO:0097159 | 0.02680 | 2.464 | 8.957 | 14 | 812 | organic cyclic compound binding |
| GO: Molecular function | GO:0016886 | 0.03275 | 46.818 | 0.033 | 1 | 3 | ligase activity, forming phosphoric ester bonds |
| GO: Molecular function | GO:0008440 | 0.04343 | 31.197 | 0.044 | 1 | 4 | inositol-1,4,5-trisphosphate 3-kinase activity |
| GO: Cellular component | GO:0043292 | 0.01958 | 106.875 | 0.020 | 1 | 2 | contractile fiber |
| GO: Cellular component | GO:0005861 | 0.01958 | 106.875 | 0.020 | 1 | 2 | troponin complex |
| GO: Cellular component | GO:0036379 | 0.01958 | 106.875 | 0.020 | 1 | 2 | myofilament |
| GO: Cellular component | GO:0030017 | 0.01958 | 106.875 | 0.020 | 1 | 2 | sarcomere |
# For flavus and niger, we additionally have to find the best BLAST Apis genes when constructing the gene lists
gene.universe.flavus.splicing <- (tbl(my_db, "isoforms_lf") %>%
group_by(gene) %>%
summarise(nIsoforms = n()) %>% filter(nIsoforms > 1) %>%
as.data.frame() %>%
dplyr::select(gene) %>% as.data.frame())[,1]
gene.universe.flavus.splicing <- (tbl(my_db, "lf2am") %>% # Convert to Apis gene names via BLAST
filter(lf %in% gene.universe.flavus.splicing) %>%
dplyr::select(am) %>% filter(!is.na(am)) %>% as.data.frame())[,1]
alt.spliced.flavus <- (tbl(my_db, "lf2am") %>%
filter(lf %in% lf.alt.splice$Gene) %>%
dplyr::select(am) %>% filter(!is.na(am)) %>% as.data.frame())[,1]
Table S23: Results of KEGG and GO enrichment analysis on the list of genes showing significant alternative splicing in L. flavus. The gene universe was defined as all genes that showed alternative splicing in L. flavus, which also had a known ortholog in A. mellifera.
GO.and.KEGG.enrichment(alt.spliced.flavus, gene.universe.flavus)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:01230 | 0.01331 | 14.889 | 0.185 | 2 | 35 | Biosynthesis of amino acids |
| KEGG | KEGG:01100 | 0.01420 | 6.619 | 2.514 | 6 | 476 | Metabolic pathways |
| KEGG | KEGG:01200 | 0.03367 | 8.800 | 0.301 | 2 | 57 | Carbon metabolism |
| KEGG | KEGG:00670 | 0.03645 | 35.738 | 0.037 | 1 | 7 | One carbon pool by folate |
| KEGG | KEGG:00061 | 0.04157 | 30.612 | 0.042 | 1 | 8 | Fatty acid biosynthesis |
| GO: Biological process | GO:0046483 | 0.00305 | 6.729 | 3.156 | 8 | 455 | heterocycle metabolic process |
| GO: Biological process | GO:0006725 | 0.00309 | 6.708 | 3.163 | 8 | 456 | cellular aromatic compound metabolic process |
| GO: Biological process | GO:1901360 | 0.00329 | 6.625 | 3.190 | 8 | 460 | organic cyclic compound metabolic process |
| GO: Biological process | GO:0051187 | 0.00694 | Inf | 0.007 | 1 | 1 | cofactor catabolic process |
| GO: Biological process | GO:0003012 | 0.00694 | Inf | 0.007 | 1 | 1 | muscle system process |
| GO: Biological process | GO:0006788 | 0.00694 | Inf | 0.007 | 1 | 1 | heme oxidation |
| GO: Biological process | GO:0006937 | 0.00694 | Inf | 0.007 | 1 | 1 | regulation of muscle contraction |
| GO: Biological process | GO:0033015 | 0.00694 | Inf | 0.007 | 1 | 1 | tetrapyrrole catabolic process |
| GO: Biological process | GO:0032264 | 0.00694 | Inf | 0.007 | 1 | 1 | IMP salvage |
| GO: Biological process | GO:0009126 | 0.01298 | 14.361 | 0.180 | 2 | 26 | purine nucleoside monophosphate metabolic process |
| GO: Biological process | GO:0035999 | 0.01383 | 157.400 | 0.014 | 1 | 2 | tetrahydrofolate interconversion |
| GO: Biological process | GO:0044057 | 0.01383 | 157.400 | 0.014 | 1 | 2 | regulation of system process |
| GO: Biological process | GO:0009161 | 0.01712 | 12.278 | 0.208 | 2 | 30 | ribonucleoside monophosphate metabolic process |
| GO: Biological process | GO:0006163 | 0.01823 | 11.847 | 0.215 | 2 | 31 | purine nucleotide metabolic process |
| GO: Biological process | GO:0006760 | 0.02068 | 78.650 | 0.021 | 1 | 3 | folic acid-containing compound metabolic process |
| GO: Biological process | GO:0006544 | 0.02068 | 78.650 | 0.021 | 1 | 3 | glycine metabolic process |
| GO: Biological process | GO:0043101 | 0.02068 | 78.650 | 0.021 | 1 | 3 | purine-containing compound salvage |
| GO: Biological process | GO:0009259 | 0.02297 | 10.384 | 0.243 | 2 | 35 | ribonucleotide metabolic process |
| GO: Biological process | GO:0008152 | 0.02409 | 7.138 | 6.443 | 10 | 929 | metabolic process |
| GO: Biological process | GO:2001141 | 0.02555 | 5.908 | 0.673 | 3 | 97 | regulation of RNA biosynthetic process |
| GO: Biological process | GO:0006355 | 0.02555 | 5.908 | 0.673 | 3 | 97 | regulation of transcription, DNA-templated |
| GO: Biological process | GO:0006165 | 0.02748 | 52.400 | 0.028 | 1 | 4 | nucleoside diphosphate phosphorylation |
| GO: Biological process | GO:0006563 | 0.02748 | 52.400 | 0.028 | 1 | 4 | L-serine metabolic process |
| GO: Biological process | GO:0046040 | 0.02748 | 52.400 | 0.028 | 1 | 4 | IMP metabolic process |
| GO: Biological process | GO:0006096 | 0.02748 | 52.400 | 0.028 | 1 | 4 | glycolytic process |
| GO: Biological process | GO:0043173 | 0.02748 | 52.400 | 0.028 | 1 | 4 | nucleotide salvage |
| GO: Biological process | GO:0019219 | 0.02770 | 5.714 | 0.694 | 3 | 100 | regulation of nucleobase-containing compound metabolic process |
| GO: Biological process | GO:0051186 | 0.03084 | 8.884 | 0.285 | 2 | 45 | cofactor metabolic process |
| GO: Biological process | GO:0006778 | 0.03424 | 39.275 | 0.035 | 1 | 5 | porphyrin-containing compound metabolic process |
| GO: Biological process | GO:0009889 | 0.03640 | 5.094 | 0.770 | 3 | 111 | regulation of biosynthetic process |
| GO: Biological process | GO:0009185 | 0.04096 | 31.400 | 0.042 | 1 | 6 | ribonucleoside diphosphate metabolic process |
| GO: Biological process | GO:0009135 | 0.04096 | 31.400 | 0.042 | 1 | 6 | purine nucleoside diphosphate metabolic process |
| GO: Biological process | GO:0046031 | 0.04096 | 31.400 | 0.042 | 1 | 6 | ADP metabolic process |
| GO: Biological process | GO:0016052 | 0.04096 | 31.400 | 0.042 | 1 | 6 | carbohydrate catabolic process |
| GO: Biological process | GO:0060255 | 0.04546 | 4.630 | 0.839 | 3 | 121 | regulation of macromolecule metabolic process |
| GO: Biological process | GO:0042440 | 0.04764 | 26.150 | 0.049 | 1 | 7 | pigment metabolic process |
| GO: Biological process | GO:0034641 | 0.04855 | 3.298 | 3.835 | 7 | 553 | cellular nitrogen compound metabolic process |
| GO: Molecular function | GO:0004392 | 0.00539 | Inf | 0.005 | 1 | 1 | heme oxygenase (decyclizing) activity |
| GO: Molecular function | GO:0004372 | 0.00539 | Inf | 0.005 | 1 | 1 | glycine hydroxymethyltransferase activity |
| GO: Molecular function | GO:0004332 | 0.00539 | Inf | 0.005 | 1 | 1 | fructose-bisphosphate aldolase activity |
| GO: Molecular function | GO:0003876 | 0.00539 | Inf | 0.005 | 1 | 1 | AMP deaminase activity |
| GO: Molecular function | GO:0031177 | 0.01075 | 198.692 | 0.011 | 1 | 2 | phosphopantetheine binding |
| GO: Molecular function | GO:0019239 | 0.01609 | 99.308 | 0.016 | 1 | 3 | deaminase activity |
| GO: Molecular function | GO:0004181 | 0.01609 | 99.308 | 0.016 | 1 | 3 | metallocarboxypeptidase activity |
| GO: Molecular function | GO:0016814 | 0.02139 | 66.179 | 0.022 | 1 | 4 | hydrolase activity, acting on carbon-nitrogen (but not peptide) bonds, in cyclic amidines |
| GO: Molecular function | GO:0004402 | 0.02139 | 66.179 | 0.022 | 1 | 4 | histone acetyltransferase activity |
| GO: Molecular function | GO:0034212 | 0.02668 | 49.615 | 0.027 | 1 | 5 | peptide N-acetyltransferase activity |
| GO: Molecular function | GO:0003690 | 0.02668 | 49.615 | 0.027 | 1 | 5 | double-stranded DNA binding |
| GO: Cellular component | GO:0043292 | 0.00845 | 264.625 | 0.008 | 1 | 2 | contractile fiber |
| GO: Cellular component | GO:0005861 | 0.00845 | 264.625 | 0.008 | 1 | 2 | troponin complex |
| GO: Cellular component | GO:0036379 | 0.00845 | 264.625 | 0.008 | 1 | 2 | myofilament |
| GO: Cellular component | GO:0030017 | 0.00845 | 264.625 | 0.008 | 1 | 2 | sarcomere |
| GO: Cellular component | GO:0005681 | 0.03751 | 32.969 | 0.038 | 1 | 9 | spliceosomal complex |
gene.universe.niger.splicing <- (tbl(my_db, "isoforms_ln") %>%
group_by(gene) %>%
summarise(nIsoforms = n()) %>% filter(nIsoforms > 1) %>%
as.data.frame() %>%
dplyr::select(gene) %>% as.data.frame())[,1]
gene.universe.niger.splicing <- (tbl(my_db, "ln2am") %>% # Convert to Apis gene names via BLAST
filter(ln %in% gene.universe.niger.splicing) %>%
dplyr::select(am) %>% filter(!is.na(am)) %>% as.data.frame())[,1] %>%
unique
alt.spliced.niger <- (tbl(my_db, "ln2am") %>%
filter(ln %in% ln.alt.splice$Gene) %>%
dplyr::select(am)%>% filter(!is.na(am)) %>% as.data.frame())[,1]
Table S24: Results of KEGG and GO enrichment analysis on the list of genes showing significant alternative splicing in L. niger. The gene universe was defined as all genes that showed alternative splicing in L. niger, which also had a known ortholog in A. mellifera.
GO.and.KEGG.enrichment(alt.spliced.niger, gene.universe.niger.splicing)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:00760 | 0.00495 | 27.000 | 0.113 | 2 | 7 | Nicotinate and nicotinamide metabolism |
| KEGG | KEGG:04745 | 0.00832 | 19.254 | 0.145 | 2 | 9 | Phototransduction - fly |
| KEGG | KEGG:00630 | 0.02003 | 11.185 | 0.226 | 2 | 14 | Glyoxylate and dicarboxylate metabolism |
| KEGG | KEGG:04391 | 0.04708 | 6.667 | 0.355 | 2 | 22 | Hippo signaling pathway - fly |
| GO: Biological process | GO:0019363 | 0.00237 | 45.193 | 0.080 | 2 | 5 | pyridine nucleotide biosynthetic process |
| GO: Biological process | GO:0072524 | 0.01463 | 13.484 | 0.192 | 2 | 12 | pyridine-containing compound metabolic process |
| GO: Biological process | GO:0035999 | 0.01601 | Inf | 0.016 | 1 | 1 | tetrahydrofolate interconversion |
| GO: Biological process | GO:0072583 | 0.01601 | Inf | 0.016 | 1 | 1 | clathrin-dependent endocytosis |
| GO: Biological process | GO:0035023 | 0.01978 | 11.219 | 0.224 | 2 | 14 | regulation of Rho protein signal transduction |
| GO: Biological process | GO:0051186 | 0.02548 | 5.496 | 0.656 | 3 | 41 | cofactor metabolic process |
| GO: Biological process | GO:0006733 | 0.02559 | 9.602 | 0.256 | 2 | 16 | oxidoreduction coenzyme metabolic process |
| GO: Biological process | GO:0019674 | 0.03031 | 67.842 | 0.031 | 1 | 2 | NAD metabolic process |
| GO: Biological process | GO:0006760 | 0.03177 | 64.500 | 0.032 | 1 | 2 | folic acid-containing compound metabolic process |
| GO: Biological process | GO:0006741 | 0.03177 | 64.500 | 0.032 | 1 | 2 | NADP biosynthetic process |
| GO: Biological process | GO:0009435 | 0.03177 | 64.500 | 0.032 | 1 | 2 | NAD biosynthetic process |
| GO: Biological process | GO:0006563 | 0.03177 | 64.500 | 0.032 | 1 | 2 | L-serine metabolic process |
| GO: Biological process | GO:0007205 | 0.03177 | 64.500 | 0.032 | 1 | 2 | protein kinase C-activating G-protein coupled receptor signaling pathway |
| GO: Biological process | GO:0007265 | 0.04268 | 7.047 | 0.336 | 2 | 21 | Ras protein signal transduction |
| GO: Biological process | GO:0006544 | 0.04729 | 32.225 | 0.048 | 1 | 3 | glycine metabolic process |
| GO: Molecular function | GO:0005093 | 0.01869 | Inf | 0.019 | 1 | 1 | Rab GDP-dissociation inhibitor activity |
| GO: Molecular function | GO:0004054 | 0.01869 | Inf | 0.019 | 1 | 1 | arginine kinase activity |
| GO: Molecular function | GO:0004791 | 0.01869 | Inf | 0.019 | 1 | 1 | thioredoxin-disulfide reductase activity |
| GO: Molecular function | GO:0005391 | 0.01869 | Inf | 0.019 | 1 | 1 | sodium:potassium-exchanging ATPase activity |
| GO: Molecular function | GO:0003952 | 0.01869 | Inf | 0.019 | 1 | 1 | NAD+ synthase (glutamine-hydrolyzing) activity |
| GO: Molecular function | GO:0004372 | 0.01869 | Inf | 0.019 | 1 | 1 | glycine hydroxymethyltransferase activity |
| GO: Molecular function | GO:0005089 | 0.03068 | 8.449 | 0.280 | 2 | 15 | Rho guanyl-nucleotide exchange factor activity |
| GO: Molecular function | GO:0008237 | 0.03248 | 4.784 | 0.710 | 3 | 38 | metallopeptidase activity |
| GO: Molecular function | GO:0043167 | 0.03462 | 1.956 | 9.495 | 15 | 508 | ion binding |
| GO: Molecular function | GO:0004890 | 0.03704 | 53.821 | 0.037 | 1 | 2 | GABA-A receptor activity |
| GO: Molecular function | GO:0003994 | 0.03704 | 53.821 | 0.037 | 1 | 2 | aconitate hydratase activity |
| GO: Molecular function | GO:0003951 | 0.03704 | 53.821 | 0.037 | 1 | 2 | NAD+ kinase activity |
| GO: Molecular function | GO:0004143 | 0.03704 | 53.821 | 0.037 | 1 | 2 | diacylglycerol kinase activity |
| GO: Cellular component | GO:0005868 | 0.01476 | Inf | 0.015 | 1 | 1 | cytoplasmic dynein complex |
These two figures help to see which KEGG and GO terms showed up more than once, and to compare Apis and the two Lasius species.
# First, look for enriched KEGG and GO terms in all the DE gene and isoform lists jsut as before, but this time return all the results (keep.all = TRUE)
big.table <- rbind(suppressMessages(
GO.and.KEGG.enrichment(up.in.control.apis, gene.universe.apis, kable = FALSE, keep.all = TRUE) ) %>%
mutate(species = "A. mellifera", type = "Up in control"),
GO.and.KEGG.enrichment(up.in.QP.apis, gene.universe.apis, kable = FALSE, keep.all = TRUE) %>%
mutate(species = "A. mellifera", type = "Up in QP"),
GO.and.KEGG.enrichment(up.in.control.flavus, gene.universe.flavus, kable = FALSE, keep.all = TRUE) %>%
mutate(species = "L. flavus", type = "Up in control"),
GO.and.KEGG.enrichment(up.in.QP.flavus, gene.universe.flavus, kable = FALSE, keep.all = TRUE) %>%
mutate(species = "L. flavus", type = "Up in QP"),
GO.and.KEGG.enrichment(up.in.control.niger, gene.universe.niger, kable = FALSE, keep.all = TRUE) %>%
mutate(species = "L. niger", type = "Up in control"),
GO.and.KEGG.enrichment(up.in.QP.niger, gene.universe.niger, kable = FALSE, keep.all = TRUE) %>%
mutate(species = "L. niger", type = "Up in QP"),
GO.and.KEGG.enrichment(am.alt.splice$Gene, gene.universe.apis.splicing, kable = FALSE, keep.all = TRUE) %>%
mutate(species = "A. mellifera", type = "Splicing"),
GO.and.KEGG.enrichment(alt.spliced.flavus, gene.universe.flavus, kable = FALSE, keep.all = TRUE) %>%
mutate(species = "L. flavus", type = "Splicing"),
GO.and.KEGG.enrichment(alt.spliced.niger, gene.universe.niger.splicing, kable = FALSE, keep.all = TRUE) %>%
mutate(species = "L. niger", type = "Splicing")) %>%
filter(Test_type %in% c("KEGG", "GO: Biological process"))
# This line means that GO/KEGG categories which did not even appear in the list of enriched genes get a p value of 1
plot.data <- expand.grid(ID = unique(big.table$ID),
species = unique(big.table$species),
type = unique(big.table$type), stringsAsFactors = FALSE) %>%
left_join(big.table %>% dplyr::select(ID, type, species, Pvalue), by = c("ID", "species", "type")) %>%
mutate(Pvalue = as.numeric(as.character(replace(Pvalue, is.na(Pvalue), 1))))
Figure 2: A summary of the KEGG enrichment tests: KEGG terms with multiple red squares were significantly enriched in multiple tests. Each square shows one of three results, for one of three species, and the colour of the square indicates the p-value for that result (on a -log10 scale) - blue squares are not statistically significant, red squares are significant (and are also marked with asterisks), and white squares are close to the p = 0.05 threshold. The “Up in QP” rows show the results of enrichment tests for KEGG terms on the gene set that was significantly up-regulated in queen pheromone-treated workers. The “Up in control” row shows the same tests, on the gene set that was significantly up-regulated in control workers. The “Splicing” row shows the results of the same tests, on the gene set that showed a significant change in alterative splicing between the two treatments.
kegg.plot.data <- plot.data %>% filter(grepl("KEGG", ID))
kegg.plot.data <- kegg.plot.data[kegg.plot.data$ID %in% (kegg.plot.data %>%
group_by(ID) %>%
summarise(min.p = min(Pvalue)) %>%
filter(min.p < 0.05) %>% .$ID), ] %>%
left_join(big.table %>% select(ID, Term), by = "ID") %>%
distinct() %>% mutate(sig = " ", sig = replace(sig, Pvalue<0.05, "*"))
kegg.plot <- kegg.plot.data %>% ggplot(aes(x = species, y = type, fill = -log10(Pvalue+0.000000001))) +
geom_tile(colour="black") +
geom_text(aes(label=sig)) +
facet_wrap(~Term, labeller = labeller(Term = label_wrap_gen(30))) +
scale_fill_gradient2(name = "-log10(p)", low = "steelblue", mid = "white", high = "tomato", midpoint = -log10(0.05)) +
theme_bw() + scale_x_discrete(expand=c(0,0)) + scale_y_discrete(expand=c(0,0)) +
theme(panel.grid = element_blank(),
strip.background = element_rect(fill = "white"),
axis.text.x = element_text(face = "italic"),
legend.position = c(12/14, 1/12), legend.direction = "horizontal") +
xlab(NULL) + ylab(NULL)
ggsave(kegg.plot, file = "figures/KEGG summary fig.pdf", height = 8, width = 12)
kegg.plot
Figure 3: A summary of the GO enrichment tests: GO terms with multiple red squares were significantly enriched in multiple tests. For brevity, the figure only shows GO terms for which two or more enrichment tests returned a significant result. The figure can be interpreted as for Figure S7.
go.plot.data <- plot.data %>% filter(grepl("GO", ID))
go.plot.data <- go.plot.data[go.plot.data$ID %in% (go.plot.data %>%
group_by(ID) %>%
summarise(n.sig = sum(Pvalue<0.05)) %>%
filter(n.sig >1) %>% .$ID), ] %>%
left_join(big.table %>% select(ID, Term), by = "ID") %>% distinct() %>%
mutate(sig = " ", sig = replace(sig, Pvalue<0.05, "*"))
go.plot.data$Term <- with(go.plot.data, paste(toupper(substr(Term, 1, 1)), substr(Term, 2, nchar(Term)), sep=""))
go.plot <- go.plot.data %>%
filter(Term != "Purine nucleoside monophosphate metabolic process", # omit these 'child' GO terms for brevity
Term != "Purine nucleoside diphosphate metabolic process",
Term != "Purine nucleoside triphosphate metabolic process",
Term != "Ribonucleoside monophosphate metabolic process",
Term != "Ribonucleoside diphosphate metabolic process",
Term != "Ribonucleoside triphosphate metabolic process") %>%
ggplot(aes(x = species, y = type, fill = -log10(Pvalue + 0.000000001))) +
geom_tile(colour="black") +
geom_text(aes(label=sig)) +
facet_wrap(~Term, labeller = labeller(Term = label_wrap_gen(25))) +
scale_fill_gradient2(name = "-log10(p)", low = "steelblue", mid = "white", high = "tomato", midpoint = -log10(0.05)) +
theme_bw() + scale_x_discrete(expand=c(0,0)) + scale_y_discrete(expand=c(0,0)) +
theme(panel.grid = element_blank(),
strip.background = element_rect(fill = "white"),
axis.text.x = element_text(face = "italic"),
legend.position = c(12/14, 1/12), legend.direction = "horizontal") +
xlab(NULL) + ylab(NULL)
ggsave(go.plot, file = "figures/GO summary fig.pdf", height = 10, width = 13)
go.plot
Table S25: Results of KEGG and GO enrichment analysis for the genes in Module 1. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(1), gene.universe.modules)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:03440 | 0.00028 | 15.874 | 6.389 | 13 | 14 | Homologous recombination |
| KEGG | KEGG:03460 | 0.00119 | 13.377 | 5.477 | 11 | 12 | Fanconi anemia pathway |
| KEGG | KEGG:03420 | 0.00453 | 6.677 | 5.933 | 11 | 13 | Nucleotide excision repair |
| KEGG | KEGG:03040 | 0.00897 | 2.075 | 23.275 | 32 | 51 | Spliceosome |
| KEGG | KEGG:03430 | 0.01946 | 8.443 | 3.651 | 7 | 8 | Mismatch repair |
| GO: Biological process | GO:0090304 | 0.00000 | 2.022 | 118.799 | 153 | 256 | nucleic acid metabolic process |
| GO: Biological process | GO:0033554 | 0.00029 | 3.901 | 15.778 | 26 | 34 | cellular response to stress |
| GO: Biological process | GO:0006281 | 0.00036 | 4.106 | 14.386 | 24 | 31 | DNA repair |
| GO: Biological process | GO:0044260 | 0.00050 | 1.521 | 192.120 | 219 | 414 | cellular macromolecule metabolic process |
| GO: Biological process | GO:0006396 | 0.00147 | 2.556 | 22.393 | 33 | 49 | RNA processing |
| GO: Biological process | GO:0046483 | 0.00159 | 1.488 | 153.139 | 176 | 330 | heterocycle metabolic process |
| GO: Biological process | GO:1901360 | 0.00193 | 1.475 | 154.531 | 177 | 333 | organic cyclic compound metabolic process |
| GO: Biological process | GO:0006725 | 0.00295 | 1.450 | 153.603 | 175 | 331 | cellular aromatic compound metabolic process |
| GO: Biological process | GO:0006397 | 0.00372 | 3.119 | 13.458 | 21 | 29 | mRNA processing |
| GO: Biological process | GO:0016043 | 0.00483 | 1.819 | 41.765 | 54 | 90 | cellular component organization |
| GO: Biological process | GO:0051276 | 0.00958 | Inf | 2.773 | 6 | 6 | chromosome organization |
| GO: Biological process | GO:0009968 | 0.02130 | Inf | 2.320 | 5 | 5 | negative regulation of signal transduction |
| GO: Biological process | GO:0006310 | 0.02130 | Inf | 2.320 | 5 | 5 | DNA recombination |
| GO: Biological process | GO:0006399 | 0.02270 | 2.168 | 15.778 | 22 | 34 | tRNA metabolic process |
| GO: Biological process | GO:0016192 | 0.02379 | 1.875 | 22.739 | 30 | 49 | vesicle-mediated transport |
| GO: Biological process | GO:0009987 | 0.03746 | 1.320 | 347.536 | 360 | 769 | cellular process |
| GO: Biological process | GO:0000280 | 0.04161 | 7.000 | 3.248 | 6 | 7 | nuclear division |
| GO: Biological process | GO:0061025 | 0.04161 | 7.000 | 3.248 | 6 | 7 | membrane fusion |
| GO: Biological process | GO:0071103 | 0.04608 | Inf | 1.856 | 4 | 4 | DNA conformation change |
| GO: Biological process | GO:0043161 | 0.04608 | Inf | 1.856 | 4 | 4 | proteasome-mediated ubiquitin-dependent protein catabolic process |
| GO: Biological process | GO:0098813 | 0.04608 | Inf | 1.856 | 4 | 4 | nuclear chromosome segregation |
| GO: Biological process | GO:0000070 | 0.04608 | Inf | 1.856 | 4 | 4 | mitotic sister chromatid segregation |
| GO: Biological process | GO:0000075 | 0.04608 | Inf | 1.856 | 4 | 4 | cell cycle checkpoint |
| GO: Biological process | GO:0051304 | 0.04608 | Inf | 1.856 | 4 | 4 | chromosome separation |
| GO: Biological process | GO:0019941 | 0.04718 | 1.963 | 14.850 | 20 | 32 | modification-dependent protein catabolic process |
| GO: Biological process | GO:0006807 | 0.04937 | 1.235 | 205.114 | 219 | 442 | nitrogen compound metabolic process |
| GO: Molecular function | GO:0003676 | 0.00001 | 1.676 | 167.146 | 205 | 377 | nucleic acid binding |
| GO: Molecular function | GO:0008270 | 0.00173 | 1.649 | 70.937 | 89 | 160 | zinc ion binding |
| GO: Molecular function | GO:0005096 | 0.00177 | 7.636 | 6.207 | 12 | 14 | GTPase activator activity |
| GO: Molecular function | GO:0016811 | 0.00389 | 11.421 | 4.434 | 9 | 10 | hydrolase activity, acting on carbon-nitrogen (but not peptide) bonds, in linear amides |
| GO: Molecular function | GO:0030554 | 0.00459 | 1.448 | 107.736 | 127 | 243 | adenyl nucleotide binding |
| GO: Molecular function | GO:0005524 | 0.00566 | 1.435 | 107.293 | 126 | 242 | ATP binding |
| GO: Molecular function | GO:0016740 | 0.00648 | 1.383 | 133.007 | 153 | 300 | transferase activity |
| GO: Molecular function | GO:0008276 | 0.00751 | Inf | 2.660 | 6 | 6 | protein methyltransferase activity |
| GO: Molecular function | GO:0060589 | 0.00903 | 3.562 | 8.424 | 14 | 19 | nucleoside-triphosphatase regulator activity |
| GO: Molecular function | GO:0016779 | 0.01553 | 2.547 | 11.971 | 18 | 27 | nucleotidyltransferase activity |
| GO: Molecular function | GO:0000166 | 0.01637 | 1.281 | 182.664 | 202 | 412 | nucleotide binding |
| GO: Molecular function | GO:0008242 | 0.01701 | Inf | 2.217 | 5 | 5 | omega peptidase activity |
| GO: Molecular function | GO:0016278 | 0.01701 | Inf | 2.217 | 5 | 5 | lysine N-methyltransferase activity |
| GO: Molecular function | GO:0004725 | 0.01772 | 4.227 | 5.764 | 10 | 13 | protein tyrosine phosphatase activity |
| GO: Molecular function | GO:0035091 | 0.02205 | 3.488 | 6.650 | 11 | 15 | phosphatidylinositol binding |
| GO: Molecular function | GO:0008080 | 0.02447 | 5.064 | 4.434 | 8 | 10 | N-acetyltransferase activity |
| GO: Molecular function | GO:0046872 | 0.02640 | 1.257 | 174.683 | 192 | 394 | metal ion binding |
| GO: Molecular function | GO:1901363 | 0.03293 | 1.275 | 137.137 | 152 | 330 | heterocyclic compound binding |
| GO: Molecular function | GO:0097159 | 0.03293 | 1.275 | 137.137 | 152 | 330 | organic cyclic compound binding |
| GO: Molecular function | GO:0036459 | 0.03762 | 3.167 | 6.207 | 10 | 14 | thiol-dependent ubiquitinyl hydrolase activity |
| GO: Molecular function | GO:0018024 | 0.03847 | Inf | 1.773 | 4 | 4 | histone-lysine N-methyltransferase activity |
| GO: Molecular function | GO:0003690 | 0.03847 | Inf | 1.773 | 4 | 4 | double-stranded DNA binding |
| GO: Molecular function | GO:0004386 | 0.04042 | 2.080 | 12.857 | 18 | 29 | helicase activity |
| GO: Molecular function | GO:0016875 | 0.04266 | 2.788 | 7.094 | 11 | 16 | ligase activity, forming carbon-oxygen bonds |
| GO: Molecular function | GO:0004812 | 0.04266 | 2.788 | 7.094 | 11 | 16 | aminoacyl-tRNA ligase activity |
| GO: Molecular function | GO:0004672 | 0.04337 | 1.550 | 32.365 | 40 | 73 | protein kinase activity |
| GO: Cellular component | GO:0005623 | 0.00008 | 1.529 | 319.265 | 354 | 776 | cell |
| GO: Cellular component | GO:0043227 | 0.00072 | 1.496 | 146.879 | 173 | 357 | membrane-bounded organelle |
| GO: Cellular component | GO:0005681 | 0.00080 | Inf | 3.291 | 8 | 8 | spliceosomal complex |
| GO: Cellular component | GO:0005634 | 0.00262 | 1.592 | 71.381 | 89 | 179 | nucleus |
| GO: Cellular component | GO:0005622 | 0.00263 | 1.773 | 45.593 | 60 | 124 | intracellular |
| GO: Cellular component | GO:0043229 | 0.00292 | 1.384 | 189.667 | 214 | 461 | intracellular organelle |
| GO: Cellular component | GO:0000151 | 0.01004 | 10.126 | 3.291 | 7 | 8 | ubiquitin ligase complex |
| GO: Cellular component | GO:0044428 | 0.01102 | 1.930 | 23.117 | 32 | 57 | nuclear part |
| GO: Cellular component | GO:0005694 | 0.01119 | Inf | 2.040 | 5 | 5 | chromosome |
| GO: Cellular component | GO:0044424 | 0.01126 | 1.570 | 50.614 | 63 | 132 | intracellular part |
| GO: Cellular component | GO:0043234 | 0.01314 | 1.433 | 78.399 | 93 | 192 | protein complex |
| GO: Cellular component | GO:0005875 | 0.02123 | 3.623 | 5.760 | 10 | 14 | microtubule associated complex |
| GO: Cellular component | GO:0000228 | 0.02916 | 5.057 | 3.703 | 7 | 9 | nuclear chromosome |
| GO: Cellular component | GO:0044427 | 0.04213 | 2.655 | 6.994 | 11 | 17 | chromosomal part |
| GO: Cellular component | GO:0031011 | 0.04612 | 7.207 | 2.469 | 5 | 6 | Ino80 complex |
| GO: Cellular component | GO:0044422 | 0.04686 | 1.314 | 79.816 | 91 | 194 | organelle part |
Table S26: Results of KEGG and GO enrichment analysis for the genes in Module 2. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(2), gene.universe.modules)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:03010 | 0.00000 | 13.284 | 12.037 | 43 | 58 | Ribosome |
| KEGG | KEGG:03050 | 0.00426 | 3.170 | 5.603 | 12 | 27 | Proteasome |
| KEGG | KEGG:00051 | 0.00538 | 9.740 | 1.453 | 5 | 7 | Fructose and mannose metabolism |
| KEGG | KEGG:00590 | 0.00759 | 15.532 | 1.038 | 4 | 5 | Arachidonic acid metabolism |
| KEGG | KEGG:04150 | 0.04175 | 2.048 | 7.264 | 12 | 35 | mTOR signaling pathway |
| GO: Biological process | GO:0006518 | 0.00000 | 5.801 | 16.624 | 46 | 87 | peptide metabolic process |
| GO: Biological process | GO:0043604 | 0.00000 | 5.789 | 16.242 | 45 | 85 | amide biosynthetic process |
| GO: Biological process | GO:0006412 | 0.00000 | 5.370 | 15.548 | 42 | 82 | translation |
| GO: Biological process | GO:1901566 | 0.00000 | 3.395 | 27.134 | 56 | 142 | organonitrogen compound biosynthetic process |
| GO: Biological process | GO:0009059 | 0.00064 | 1.798 | 43.949 | 62 | 230 | macromolecule biosynthetic process |
| GO: Biological process | GO:0018193 | 0.00281 | 6.097 | 2.293 | 7 | 12 | peptidyl-amino acid modification |
| GO: Biological process | GO:0044249 | 0.01080 | 1.484 | 58.911 | 73 | 312 | cellular biosynthetic process |
| GO: Biological process | GO:0034641 | 0.02782 | 1.367 | 76.433 | 89 | 400 | cellular nitrogen compound metabolic process |
| GO: Biological process | GO:0071704 | 0.02957 | 1.362 | 120.382 | 133 | 630 | organic substance metabolic process |
| GO: Biological process | GO:0006457 | 0.03428 | 2.443 | 4.777 | 9 | 25 | protein folding |
| GO: Biological process | GO:0044267 | 0.03616 | 1.674 | 15.210 | 22 | 93 | cellular protein metabolic process |
| GO: Biological process | GO:0006414 | 0.03637 | Inf | 0.382 | 2 | 2 | translational elongation |
| GO: Biological process | GO:0044205 | 0.03637 | Inf | 0.382 | 2 | 2 | ‘de novo’ UMP biosynthetic process |
| GO: Biological process | GO:0018095 | 0.03637 | Inf | 0.382 | 2 | 2 | protein polyglutamylation |
| GO: Biological process | GO:0044712 | 0.03981 | 2.752 | 3.439 | 7 | 18 | single-organism catabolic process |
| GO: Biological process | GO:0044238 | 0.04036 | 1.327 | 112.166 | 124 | 587 | primary metabolic process |
| GO: Biological process | GO:0044272 | 0.04783 | 4.296 | 1.529 | 4 | 8 | sulfur compound biosynthetic process |
| GO: Molecular function | GO:0003735 | 0.00000 | 13.498 | 9.757 | 40 | 56 | structural constituent of ribosome |
| GO: Molecular function | GO:0004298 | 0.00140 | 9.650 | 1.568 | 6 | 9 | threonine-type endopeptidase activity |
| GO: Molecular function | GO:0016491 | 0.00767 | 1.679 | 26.310 | 38 | 151 | oxidoreductase activity |
| GO: Molecular function | GO:0019843 | 0.01827 | 14.350 | 0.697 | 3 | 4 | rRNA binding |
| GO: Molecular function | GO:0016209 | 0.01832 | 4.802 | 1.742 | 5 | 10 | antioxidant activity |
| GO: Molecular function | GO:0050660 | 0.02528 | 3.064 | 3.136 | 7 | 18 | flavin adenine dinucleotide binding |
| GO: Molecular function | GO:0016635 | 0.03028 | Inf | 0.348 | 2 | 2 | oxidoreductase activity, acting on the CH-CH group of donors, quinone or related compound as acceptor |
| GO: Molecular function | GO:0052689 | 0.04262 | 3.425 | 2.091 | 5 | 12 | carboxylic ester hydrolase activity |
| GO: Molecular function | GO:0008135 | 0.04366 | 2.407 | 4.182 | 8 | 24 | translation factor activity, RNA binding |
| GO: Cellular component | GO:0005840 | 0.00000 | 11.975 | 10.542 | 41 | 60 | ribosome |
| GO: Cellular component | GO:1990904 | 0.00000 | 6.453 | 16.516 | 50 | 94 | ribonucleoprotein complex |
| GO: Cellular component | GO:0043228 | 0.00000 | 3.175 | 23.896 | 50 | 136 | non-membrane-bounded organelle |
| GO: Cellular component | GO:0005839 | 0.00146 | 9.595 | 1.581 | 6 | 9 | proteasome core complex |
| GO: Cellular component | GO:0015935 | 0.00146 | 9.595 | 1.581 | 6 | 9 | small ribosomal subunit |
| GO: Cellular component | GO:0005737 | 0.00261 | 2.129 | 14.512 | 25 | 99 | cytoplasm |
| GO: Cellular component | GO:0015934 | 0.00537 | Inf | 0.527 | 3 | 3 | large ribosomal subunit |
| GO: Cellular component | GO:1905369 | 0.00999 | 4.785 | 2.108 | 6 | 12 | endopeptidase complex |
| GO: Cellular component | GO:0043229 | 0.01555 | 1.387 | 81.000 | 96 | 461 | intracellular organelle |
| GO: Cellular component | GO:0005732 | 0.03077 | Inf | 0.351 | 2 | 2 | small nucleolar ribonucleoprotein complex |
| GO: Cellular component | GO:0005615 | 0.03620 | 4.753 | 1.406 | 4 | 8 | extracellular space |
| GO: Cellular component | GO:0044444 | 0.04860 | 1.509 | 20.765 | 28 | 136 | cytoplasmic part |
Table S27: Results of KEGG and GO enrichment analysis for the genes in Module 3. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(3), gene.universe.modules)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04080 | 0.00001 | 24.165 | 0.576 | 6 | 11 | Neuroactive ligand-receptor interaction |
| KEGG | KEGG:00020 | 0.00964 | 5.916 | 0.890 | 4 | 17 | Citrate cycle (TCA cycle) |
| KEGG | KEGG:00130 | 0.01509 | 18.727 | 0.209 | 2 | 4 | Ubiquinone and other terpenoid-quinone biosynthesis |
| KEGG | KEGG:01200 | 0.01696 | 3.351 | 2.146 | 6 | 41 | Carbon metabolism |
| KEGG | KEGG:04013 | 0.01961 | 3.720 | 1.623 | 5 | 31 | MAPK signaling pathway - fly |
| KEGG | KEGG:00350 | 0.02431 | 12.473 | 0.262 | 2 | 5 | Tyrosine metabolism |
| GO: Biological process | GO:0023052 | 0.00000 | 4.609 | 11.210 | 31 | 154 | signaling |
| GO: Biological process | GO:0044763 | 0.00000 | 3.199 | 29.517 | 50 | 414 | single-organism cellular process |
| GO: Biological process | GO:0050896 | 0.00000 | 3.298 | 14.195 | 31 | 195 | response to stimulus |
| GO: Biological process | GO:0050789 | 0.00000 | 3.052 | 19.727 | 38 | 271 | regulation of biological process |
| GO: Biological process | GO:0035556 | 0.00001 | 4.078 | 7.061 | 20 | 97 | intracellular signal transduction |
| GO: Biological process | GO:0007265 | 0.00021 | 8.047 | 1.383 | 7 | 19 | Ras protein signal transduction |
| GO: Biological process | GO:0051056 | 0.00030 | 7.420 | 1.456 | 7 | 20 | regulation of small GTPase mediated signal transduction |
| GO: Biological process | GO:0007218 | 0.00037 | Inf | 0.218 | 3 | 3 | neuropeptide signaling pathway |
| GO: Biological process | GO:0009966 | 0.00068 | 5.280 | 2.111 | 8 | 29 | regulation of signal transduction |
| GO: Biological process | GO:0007165 | 0.00131 | 4.149 | 2.841 | 9 | 48 | signal transduction |
| GO: Biological process | GO:0035023 | 0.00146 | 8.425 | 0.946 | 5 | 13 | regulation of Rho protein signal transduction |
| GO: Biological process | GO:0007267 | 0.02266 | 6.578 | 0.655 | 3 | 9 | cell-cell signaling |
| GO: Biological process | GO:0099537 | 0.02852 | 13.038 | 0.291 | 2 | 4 | trans-synaptic signaling |
| GO: Biological process | GO:0006836 | 0.02852 | 13.038 | 0.291 | 2 | 4 | neurotransmitter transport |
| GO: Biological process | GO:0007268 | 0.02852 | 13.038 | 0.291 | 2 | 4 | chemical synaptic transmission |
| GO: Biological process | GO:0006099 | 0.03070 | 5.633 | 0.728 | 3 | 10 | tricarboxylic acid cycle |
| GO: Biological process | GO:0008219 | 0.04531 | 8.684 | 0.364 | 2 | 5 | cell death |
| GO: Biological process | GO:0006915 | 0.04531 | 8.684 | 0.364 | 2 | 5 | apoptotic process |
| GO: Molecular function | GO:0015267 | 0.00000 | 17.267 | 2.176 | 14 | 22 | channel activity |
| GO: Molecular function | GO:0005216 | 0.00000 | 17.267 | 2.176 | 14 | 22 | ion channel activity |
| GO: Molecular function | GO:0060089 | 0.00000 | 6.818 | 5.440 | 22 | 55 | molecular transducer activity |
| GO: Molecular function | GO:0038023 | 0.00000 | 6.199 | 4.649 | 18 | 47 | signaling receptor activity |
| GO: Molecular function | GO:0005230 | 0.00000 | 38.171 | 0.989 | 8 | 10 | extracellular ligand-gated ion channel activity |
| GO: Molecular function | GO:0022891 | 0.00002 | 3.691 | 6.924 | 19 | 70 | substrate-specific transmembrane transporter activity |
| GO: Molecular function | GO:0005215 | 0.00004 | 2.893 | 11.078 | 25 | 112 | transporter activity |
| GO: Molecular function | GO:0005234 | 0.00009 | Inf | 0.396 | 4 | 4 | extracellular-glutamate-gated ion channel activity |
| GO: Molecular function | GO:0004970 | 0.00009 | Inf | 0.396 | 4 | 4 | ionotropic glutamate receptor activity |
| GO: Molecular function | GO:0022835 | 0.00009 | Inf | 0.396 | 4 | 4 | transmitter-gated channel activity |
| GO: Molecular function | GO:0099600 | 0.00029 | 4.429 | 3.415 | 11 | 36 | transmembrane receptor activity |
| GO: Molecular function | GO:0004930 | 0.00037 | 5.352 | 2.473 | 9 | 25 | G-protein coupled receptor activity |
| GO: Molecular function | GO:0004889 | 0.00095 | Inf | 0.297 | 3 | 3 | acetylcholine-activated cation-selective channel activity |
| GO: Molecular function | GO:0022834 | 0.00109 | 19.085 | 0.581 | 4 | 6 | ligand-gated channel activity |
| GO: Molecular function | GO:0005267 | 0.00118 | 18.631 | 0.593 | 4 | 6 | potassium channel activity |
| GO: Molecular function | GO:0005085 | 0.00287 | 4.706 | 2.077 | 7 | 21 | guanyl-nucleotide exchange factor activity |
| GO: Molecular function | GO:0005089 | 0.00595 | 5.835 | 1.286 | 5 | 13 | Rho guanyl-nucleotide exchange factor activity |
| GO: Molecular function | GO:0048038 | 0.00973 | Inf | 0.198 | 2 | 2 | quinone binding |
| GO: Molecular function | GO:0015291 | 0.01205 | 6.194 | 0.989 | 4 | 10 | secondary active transmembrane transporter activity |
| GO: Molecular function | GO:0046873 | 0.01317 | 3.740 | 2.077 | 6 | 21 | metal ion transmembrane transporter activity |
| GO: Molecular function | GO:0015294 | 0.01519 | 9.254 | 0.593 | 3 | 6 | solute:cation symporter activity |
| GO: Molecular function | GO:0005509 | 0.01607 | 2.484 | 4.748 | 10 | 48 | calcium ion binding |
| GO: Molecular function | GO:0042302 | 0.01750 | 5.306 | 1.088 | 4 | 11 | structural constituent of cuticle |
| GO: Molecular function | GO:0005328 | 0.02729 | 18.424 | 0.297 | 2 | 3 | neurotransmitter:sodium symporter activity |
| GO: Molecular function | GO:0016849 | 0.03665 | 5.546 | 0.791 | 3 | 8 | phosphorus-oxygen lyase activity |
| GO: Molecular function | GO:0004857 | 0.03665 | 5.546 | 0.791 | 3 | 8 | enzyme inhibitor activity |
| GO: Molecular function | GO:0019887 | 0.03665 | 5.546 | 0.791 | 3 | 8 | protein kinase regulator activity |
| GO: Molecular function | GO:0015077 | 0.03686 | 2.796 | 2.572 | 6 | 26 | monovalent inorganic cation transmembrane transporter activity |
| GO: Molecular function | GO:0008324 | 0.04009 | 2.305 | 3.998 | 8 | 41 | cation transmembrane transporter activity |
| GO: Molecular function | GO:0004674 | 0.04050 | 3.098 | 1.978 | 5 | 20 | protein serine/threonine kinase activity |
| GO: Cellular component | GO:0044456 | 0.00000 | Inf | 0.776 | 7 | 7 | synapse part |
| GO: Cellular component | GO:0045211 | 0.00000 | Inf | 0.785 | 7 | 7 | postsynaptic membrane |
| GO: Cellular component | GO:0098590 | 0.00000 | 58.034 | 0.897 | 7 | 8 | plasma membrane region |
| GO: Cellular component | GO:0030054 | 0.00000 | 22.222 | 1.233 | 8 | 11 | cell junction |
| GO: Cellular component | GO:0016021 | 0.00003 | 2.023 | 70.047 | 94 | 625 | integral component of membrane |
| GO: Cellular component | GO:0044425 | 0.00012 | 1.916 | 73.970 | 96 | 660 | membrane part |
| GO: Cellular component | GO:0098793 | 0.01249 | Inf | 0.224 | 2 | 2 | presynapse |
| GO: Cellular component | GO:0005886 | 0.01638 | 3.156 | 2.799 | 7 | 26 | plasma membrane |
| GO: Cellular component | GO:0005576 | 0.01871 | 2.329 | 5.604 | 11 | 50 | extracellular region |
Table S28: Results of KEGG and GO enrichment analysis for the genes in Module 4. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(4), gene.universe.modules)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04141 | 0.00000 | 4.973 | 7.152 | 22 | 59 | Protein processing in endoplasmic reticulum |
| KEGG | KEGG:01200 | 0.00003 | 4.591 | 4.970 | 15 | 41 | Carbon metabolism |
| KEGG | KEGG:01212 | 0.00014 | 6.929 | 2.303 | 9 | 19 | Fatty acid metabolism |
| KEGG | KEGG:01100 | 0.00084 | 1.857 | 41.455 | 58 | 342 | Metabolic pathways |
| KEGG | KEGG:01040 | 0.00094 | 29.875 | 0.606 | 4 | 5 | Biosynthesis of unsaturated fatty acids |
| KEGG | KEGG:01230 | 0.00094 | 4.276 | 3.394 | 10 | 28 | Biosynthesis of amino acids |
| KEGG | KEGG:00030 | 0.00141 | 7.548 | 1.455 | 6 | 12 | Pentose phosphate pathway |
| KEGG | KEGG:04512 | 0.00540 | 9.938 | 0.848 | 4 | 7 | ECM-receptor interaction |
| KEGG | KEGG:00061 | 0.00540 | 9.938 | 0.848 | 4 | 7 | Fatty acid biosynthesis |
| KEGG | KEGG:00500 | 0.00978 | 7.445 | 0.970 | 4 | 8 | Starch and sucrose metabolism |
| KEGG | KEGG:03050 | 0.01125 | 3.185 | 3.273 | 8 | 27 | Proteasome |
| KEGG | KEGG:00260 | 0.01394 | 4.670 | 1.576 | 5 | 13 | Glycine, serine and threonine metabolism |
| KEGG | KEGG:00565 | 0.01449 | 11.105 | 0.606 | 3 | 5 | Ether lipid metabolism |
| KEGG | KEGG:03060 | 0.01598 | 5.950 | 1.091 | 4 | 9 | Protein export |
| KEGG | KEGG:00520 | 0.02014 | 3.458 | 2.303 | 6 | 19 | Amino sugar and nucleotide sugar metabolism |
| KEGG | KEGG:00062 | 0.02643 | 7.395 | 0.727 | 3 | 6 | Fatty acid elongation |
| KEGG | KEGG:00280 | 0.03283 | 2.990 | 2.545 | 6 | 21 | Valine, leucine and isoleucine degradation |
| KEGG | KEGG:00510 | 0.03447 | 4.241 | 1.333 | 4 | 11 | N-Glycan biosynthesis |
| GO: Biological process | GO:0043436 | 0.00000 | 6.352 | 6.248 | 23 | 63 | oxoacid metabolic process |
| GO: Biological process | GO:0044283 | 0.00000 | 8.797 | 2.538 | 12 | 26 | small molecule biosynthetic process |
| GO: Biological process | GO:1901607 | 0.00080 | 11.851 | 0.893 | 5 | 9 | alpha-amino acid biosynthetic process |
| GO: Biological process | GO:0006544 | 0.00095 | Inf | 0.298 | 3 | 3 | glycine metabolic process |
| GO: Biological process | GO:0046394 | 0.00122 | 9.919 | 0.953 | 5 | 10 | carboxylic acid biosynthetic process |
| GO: Biological process | GO:0055086 | 0.00134 | 3.024 | 5.951 | 14 | 60 | nucleobase-containing small molecule metabolic process |
| GO: Biological process | GO:0044723 | 0.00144 | 5.593 | 1.884 | 7 | 19 | single-organism carbohydrate metabolic process |
| GO: Biological process | GO:0006633 | 0.00147 | 9.471 | 0.992 | 5 | 10 | fatty acid biosynthetic process |
| GO: Biological process | GO:0032787 | 0.00225 | 8.094 | 1.067 | 5 | 11 | monocarboxylic acid metabolic process |
| GO: Biological process | GO:0044281 | 0.00245 | 3.062 | 4.970 | 12 | 60 | small molecule metabolic process |
| GO: Biological process | GO:0072524 | 0.00393 | 6.751 | 1.190 | 5 | 12 | pyridine-containing compound metabolic process |
| GO: Biological process | GO:0046496 | 0.00393 | 6.751 | 1.190 | 5 | 12 | nicotinamide nucleotide metabolic process |
| GO: Biological process | GO:0019637 | 0.00690 | 2.348 | 7.736 | 15 | 78 | organophosphate metabolic process |
| GO: Biological process | GO:0009069 | 0.00762 | 14.388 | 0.484 | 3 | 5 | serine family amino acid metabolic process |
| GO: Biological process | GO:0006098 | 0.00819 | 13.981 | 0.496 | 3 | 5 | pentose-phosphate shunt |
| GO: Biological process | GO:0006081 | 0.00819 | 13.981 | 0.496 | 3 | 5 | cellular aldehyde metabolic process |
| GO: Biological process | GO:0006487 | 0.00976 | Inf | 0.198 | 2 | 2 | protein N-linked glycosylation |
| GO: Biological process | GO:0006890 | 0.00976 | Inf | 0.198 | 2 | 2 | retrograde vesicle-mediated transport, Golgi to ER |
| GO: Biological process | GO:0034637 | 0.00976 | Inf | 0.198 | 2 | 2 | cellular carbohydrate biosynthetic process |
| GO: Biological process | GO:0006564 | 0.00976 | Inf | 0.198 | 2 | 2 | L-serine biosynthetic process |
| GO: Biological process | GO:0009186 | 0.00976 | Inf | 0.198 | 2 | 2 | deoxyribonucleoside diphosphate metabolic process |
| GO: Biological process | GO:0072350 | 0.00976 | Inf | 0.198 | 2 | 2 | tricarboxylic acid metabolic process |
| GO: Biological process | GO:0009117 | 0.01001 | 2.598 | 5.157 | 11 | 52 | nucleotide metabolic process |
| GO: Biological process | GO:0006732 | 0.01019 | 4.894 | 1.440 | 5 | 15 | coenzyme metabolic process |
| GO: Biological process | GO:1901576 | 0.01144 | 1.661 | 31.143 | 42 | 319 | organic substance biosynthetic process |
| GO: Biological process | GO:0043413 | 0.01201 | 6.248 | 0.992 | 4 | 10 | macromolecule glycosylation |
| GO: Biological process | GO:0006796 | 0.01390 | 2.130 | 8.331 | 15 | 84 | phosphate-containing compound metabolic process |
| GO: Biological process | GO:0008652 | 0.01451 | 9.490 | 0.585 | 3 | 6 | cellular amino acid biosynthetic process |
| GO: Biological process | GO:0006090 | 0.01520 | 9.311 | 0.595 | 3 | 6 | pyruvate metabolic process |
| GO: Biological process | GO:0006733 | 0.01568 | 4.279 | 1.587 | 5 | 16 | oxidoreduction coenzyme metabolic process |
| GO: Biological process | GO:0044255 | 0.01737 | 2.825 | 3.471 | 8 | 35 | cellular lipid metabolic process |
| GO: Biological process | GO:0019318 | 0.01746 | 5.350 | 1.091 | 4 | 11 | hexose metabolic process |
| GO: Biological process | GO:1901135 | 0.02290 | 2.030 | 8.034 | 14 | 81 | carbohydrate derivative metabolic process |
| GO: Biological process | GO:0009101 | 0.02422 | 4.676 | 1.190 | 4 | 12 | glycoprotein biosynthetic process |
| GO: Biological process | GO:0046148 | 0.02736 | 18.486 | 0.298 | 2 | 3 | pigment biosynthetic process |
| GO: Biological process | GO:0035384 | 0.02736 | 18.486 | 0.298 | 2 | 3 | thioester biosynthetic process |
| GO: Biological process | GO:0009133 | 0.02736 | 18.486 | 0.298 | 2 | 3 | nucleoside diphosphate biosynthetic process |
| GO: Biological process | GO:0006094 | 0.02736 | 18.486 | 0.298 | 2 | 3 | gluconeogenesis |
| GO: Biological process | GO:0006085 | 0.02736 | 18.486 | 0.298 | 2 | 3 | acetyl-CoA biosynthetic process |
| GO: Biological process | GO:0046364 | 0.02736 | 18.486 | 0.298 | 2 | 3 | monosaccharide biosynthetic process |
| GO: Biological process | GO:0033014 | 0.02736 | 18.486 | 0.298 | 2 | 3 | tetrapyrrole biosynthetic process |
| GO: Biological process | GO:0044249 | 0.03042 | 1.529 | 31.017 | 40 | 318 | cellular biosynthetic process |
| GO: Biological process | GO:0006629 | 0.03266 | 5.865 | 0.759 | 3 | 8 | lipid metabolic process |
| GO: Biological process | GO:0044710 | 0.03957 | 3.663 | 1.345 | 4 | 19 | single-organism metabolic process |
| GO: Biological process | GO:0006520 | 0.03989 | 2.741 | 2.623 | 6 | 28 | cellular amino acid metabolic process |
| GO: Biological process | GO:0044711 | 0.04270 | 2.163 | 4.794 | 9 | 54 | single-organism biosynthetic process |
| GO: Molecular function | GO:0008483 | 0.00006 | 44.799 | 0.618 | 5 | 6 | transaminase activity |
| GO: Molecular function | GO:0016491 | 0.00091 | 2.166 | 15.543 | 28 | 151 | oxidoreductase activity |
| GO: Molecular function | GO:0030170 | 0.00248 | 5.977 | 1.544 | 6 | 15 | pyridoxal phosphate binding |
| GO: Molecular function | GO:0016620 | 0.00545 | 8.891 | 0.823 | 4 | 8 | oxidoreductase activity, acting on the aldehyde or oxo group of donors, NAD or NADP as acceptor |
| GO: Molecular function | GO:0003824 | 0.00684 | 1.553 | 75.120 | 90 | 790 | catalytic activity |
| GO: Molecular function | GO:0016616 | 0.00946 | 4.127 | 1.956 | 6 | 19 | oxidoreductase activity, acting on the CH-OH group of donors, NAD or NADP as acceptor |
| GO: Molecular function | GO:0016885 | 0.01054 | Inf | 0.206 | 2 | 2 | ligase activity, forming carbon-carbon bonds |
| GO: Molecular function | GO:0004576 | 0.01054 | Inf | 0.206 | 2 | 2 | oligosaccharyl transferase activity |
| GO: Molecular function | GO:0004185 | 0.01054 | Inf | 0.206 | 2 | 2 | serine-type carboxypeptidase activity |
| GO: Molecular function | GO:0016717 | 0.01054 | Inf | 0.206 | 2 | 2 | oxidoreductase activity, acting on paired donors, with oxidation of a pair of donors resulting in the reduction of molecular oxygen to two molecules of water |
| GO: Molecular function | GO:0052689 | 0.02773 | 4.434 | 1.235 | 4 | 12 | carboxylic ester hydrolase activity |
| GO: Molecular function | GO:0004075 | 0.02948 | 17.616 | 0.309 | 2 | 3 | biotin carboxylase activity |
| GO: Molecular function | GO:0005201 | 0.02948 | 17.616 | 0.309 | 2 | 3 | extracellular matrix structural constituent |
| GO: Molecular function | GO:0046912 | 0.02948 | 17.616 | 0.309 | 2 | 3 | transferase activity, transferring acyl groups, acyl groups converted into alkyl on transfer |
| GO: Cellular component | GO:0005783 | 0.00032 | 8.058 | 1.529 | 7 | 15 | endoplasmic reticulum |
| GO: Cellular component | GO:1905368 | 0.00152 | 6.856 | 1.427 | 6 | 14 | peptidase complex |
| GO: Cellular component | GO:0000502 | 0.00450 | 6.486 | 1.223 | 5 | 12 | proteasome complex |
| GO: Cellular component | GO:0005789 | 0.00868 | 7.223 | 0.918 | 4 | 9 | endoplasmic reticulum membrane |
| GO: Cellular component | GO:0005581 | 0.01033 | Inf | 0.204 | 2 | 2 | collagen trimer |
| GO: Cellular component | GO:0016021 | 0.01139 | 1.524 | 63.720 | 77 | 625 | integral component of membrane |
Table S29: Results of KEGG and GO enrichment analysis for the genes in Module 5. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(5), gene.universe.modules)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04120 | 0.00103 | 4.757 | 2.204 | 8 | 48 | Ubiquitin mediated proteolysis |
| KEGG | KEGG:04142 | 0.00857 | 4.699 | 1.331 | 5 | 29 | Lysosome |
| KEGG | KEGG:04144 | 0.01149 | 3.289 | 2.571 | 7 | 56 | Endocytosis |
| KEGG | KEGG:00250 | 0.04847 | 7.174 | 0.367 | 2 | 8 | Alanine, aspartate and glutamate metabolism |
| GO: Biological process | GO:0071702 | 0.00018 | 4.080 | 4.366 | 13 | 94 | organic substance transport |
| GO: Biological process | GO:0045184 | 0.00038 | 3.945 | 4.069 | 12 | 86 | establishment of protein localization |
| GO: Biological process | GO:0006886 | 0.00061 | 4.660 | 2.555 | 9 | 54 | intracellular protein transport |
| GO: Biological process | GO:0070727 | 0.00119 | 4.173 | 2.792 | 9 | 59 | cellular macromolecule localization |
| GO: Biological process | GO:0031333 | 0.00220 | Inf | 0.095 | 2 | 2 | negative regulation of protein complex assembly |
| GO: Biological process | GO:0030835 | 0.00220 | Inf | 0.095 | 2 | 2 | negative regulation of actin filament depolymerization |
| GO: Biological process | GO:0030837 | 0.00220 | Inf | 0.095 | 2 | 2 | negative regulation of actin filament polymerization |
| GO: Biological process | GO:0051016 | 0.00220 | Inf | 0.095 | 2 | 2 | barbed-end actin filament capping |
| GO: Biological process | GO:0043242 | 0.00220 | Inf | 0.095 | 2 | 2 | negative regulation of protein complex disassembly |
| GO: Biological process | GO:0051649 | 0.00243 | 3.704 | 3.076 | 9 | 65 | establishment of localization in cell |
| GO: Biological process | GO:0065008 | 0.00546 | 4.422 | 1.703 | 6 | 36 | regulation of biological quality |
| GO: Biological process | GO:0043624 | 0.00639 | 41.840 | 0.142 | 2 | 3 | cellular protein complex disassembly |
| GO: Biological process | GO:1901879 | 0.00639 | 41.840 | 0.142 | 2 | 3 | regulation of protein depolymerization |
| GO: Biological process | GO:0032984 | 0.00639 | 41.840 | 0.142 | 2 | 3 | macromolecular complex disassembly |
| GO: Biological process | GO:0010639 | 0.00639 | 41.840 | 0.142 | 2 | 3 | negative regulation of organelle organization |
| GO: Biological process | GO:0007015 | 0.00686 | 10.622 | 0.426 | 3 | 9 | actin filament organization |
| GO: Biological process | GO:0032535 | 0.00686 | 10.622 | 0.426 | 3 | 9 | regulation of cellular component size |
| GO: Biological process | GO:0032956 | 0.00686 | 10.622 | 0.426 | 3 | 9 | regulation of actin cytoskeleton organization |
| GO: Biological process | GO:0008064 | 0.00686 | 10.622 | 0.426 | 3 | 9 | regulation of actin polymerization or depolymerization |
| GO: Biological process | GO:0046033 | 0.01240 | 20.900 | 0.189 | 2 | 4 | AMP metabolic process |
| GO: Biological process | GO:0044087 | 0.01260 | 7.952 | 0.520 | 3 | 11 | regulation of cellular component biogenesis |
| GO: Biological process | GO:0032271 | 0.01260 | 7.952 | 0.520 | 3 | 11 | regulation of protein polymerization |
| GO: Biological process | GO:0043623 | 0.02042 | 6.349 | 0.615 | 3 | 13 | cellular protein complex assembly |
| GO: Biological process | GO:0030029 | 0.02042 | 6.349 | 0.615 | 3 | 13 | actin filament-based process |
| GO: Biological process | GO:0033036 | 0.02133 | 3.617 | 1.654 | 5 | 40 | macromolecule localization |
| GO: Biological process | GO:0009168 | 0.02514 | 5.766 | 0.662 | 3 | 14 | purine ribonucleoside monophosphate biosynthetic process |
| GO: Biological process | GO:0051128 | 0.03039 | 5.281 | 0.710 | 3 | 15 | regulation of cellular component organization |
| GO: Biological process | GO:0045454 | 0.03039 | 5.281 | 0.710 | 3 | 15 | cell redox homeostasis |
| GO: Biological process | GO:0046129 | 0.03617 | 4.870 | 0.757 | 3 | 16 | purine ribonucleoside biosynthetic process |
| GO: Biological process | GO:0007010 | 0.03617 | 4.870 | 0.757 | 3 | 16 | cytoskeleton organization |
| GO: Biological process | GO:0048523 | 0.04248 | 4.517 | 0.804 | 3 | 17 | negative regulation of cellular process |
| GO: Biological process | GO:0009152 | 0.04248 | 4.517 | 0.804 | 3 | 17 | purine ribonucleotide biosynthetic process |
| GO: Biological process | GO:0051125 | 0.04732 | Inf | 0.047 | 1 | 1 | regulation of actin nucleation |
| GO: Biological process | GO:0015850 | 0.04732 | Inf | 0.047 | 1 | 1 | organic hydroxy compound transport |
| GO: Biological process | GO:0009607 | 0.04732 | Inf | 0.047 | 1 | 1 | response to biotic stimulus |
| GO: Biological process | GO:0030245 | 0.04732 | Inf | 0.047 | 1 | 1 | cellulose catabolic process |
| GO: Biological process | GO:0051273 | 0.04732 | Inf | 0.047 | 1 | 1 | beta-glucan metabolic process |
| GO: Biological process | GO:0051707 | 0.04732 | Inf | 0.047 | 1 | 1 | response to other organism |
| GO: Biological process | GO:0044247 | 0.04732 | Inf | 0.047 | 1 | 1 | cellular polysaccharide catabolic process |
| GO: Biological process | GO:0042742 | 0.04732 | Inf | 0.047 | 1 | 1 | defense response to bacterium |
| GO: Biological process | GO:0006892 | 0.04732 | Inf | 0.047 | 1 | 1 | post-Golgi vesicle-mediated transport |
| GO: Biological process | GO:0006895 | 0.04732 | Inf | 0.047 | 1 | 1 | Golgi to endosome transport |
| GO: Biological process | GO:0009251 | 0.04732 | Inf | 0.047 | 1 | 1 | glucan catabolic process |
| GO: Biological process | GO:0007188 | 0.04732 | Inf | 0.047 | 1 | 1 | adenylate cyclase-modulating G-protein coupled receptor signaling pathway |
| GO: Biological process | GO:0032456 | 0.04732 | Inf | 0.047 | 1 | 1 | endocytic recycling |
| GO: Biological process | GO:2000601 | 0.04732 | Inf | 0.047 | 1 | 1 | positive regulation of Arp2/3 complex-mediated actin nucleation |
| GO: Biological process | GO:0030301 | 0.04732 | Inf | 0.047 | 1 | 1 | cholesterol transport |
| GO: Biological process | GO:0071586 | 0.04732 | Inf | 0.047 | 1 | 1 | CAAX-box protein processing |
| GO: Biological process | GO:0070271 | 0.04931 | 4.212 | 0.852 | 3 | 18 | protein complex biogenesis |
| GO: Biological process | GO:0071822 | 0.04931 | 4.212 | 0.852 | 3 | 18 | protein complex subunit organization |
| GO: Molecular function | GO:0016787 | 0.00182 | 2.171 | 15.852 | 27 | 358 | hydrolase activity |
| GO: Molecular function | GO:0042578 | 0.00628 | 4.172 | 1.727 | 6 | 39 | phosphoric ester hydrolase activity |
| GO: Molecular function | GO:0004721 | 0.01923 | 4.499 | 1.063 | 4 | 24 | phosphoprotein phosphatase activity |
| GO: Molecular function | GO:0003993 | 0.02586 | 11.053 | 0.266 | 2 | 6 | acid phosphatase activity |
| GO: Molecular function | GO:0015103 | 0.02586 | 11.053 | 0.266 | 2 | 6 | inorganic anion transmembrane transporter activity |
| GO: Molecular function | GO:0004222 | 0.02586 | 5.574 | 0.664 | 3 | 15 | metalloendopeptidase activity |
| GO: Molecular function | GO:0030170 | 0.02586 | 5.574 | 0.664 | 3 | 15 | pyridoxal phosphate binding |
| GO: Molecular function | GO:0016831 | 0.03517 | 8.837 | 0.310 | 2 | 7 | carboxy-lyase activity |
| GO: Molecular function | GO:0004018 | 0.04428 | Inf | 0.044 | 1 | 1 | N6-(1,2-dicarboxyethyl)AMP AMP-lyase (fumarate-forming) activity |
| GO: Molecular function | GO:0052855 | 0.04428 | Inf | 0.044 | 1 | 1 | ADP-dependent NAD(P)H-hydrate dehydratase activity |
| GO: Molecular function | GO:0016840 | 0.04428 | Inf | 0.044 | 1 | 1 | carbon-nitrogen lyase activity |
| GO: Molecular function | GO:0008796 | 0.04428 | Inf | 0.044 | 1 | 1 | bis(5’-nucleosyl)-tetraphosphatase activity |
| GO: Molecular function | GO:0051861 | 0.04428 | Inf | 0.044 | 1 | 1 | glycolipid binding |
| GO: Molecular function | GO:0017089 | 0.04428 | Inf | 0.044 | 1 | 1 | glycolipid transporter activity |
| GO: Molecular function | GO:0003922 | 0.04428 | Inf | 0.044 | 1 | 1 | GMP synthase (glutamine-hydrolyzing) activity |
| GO: Molecular function | GO:0008810 | 0.04428 | Inf | 0.044 | 1 | 1 | cellulase activity |
| GO: Molecular function | GO:0004532 | 0.04428 | Inf | 0.044 | 1 | 1 | exoribonuclease activity |
| GO: Molecular function | GO:0004534 | 0.04428 | Inf | 0.044 | 1 | 1 | 5’-3’ exoribonuclease activity |
| GO: Molecular function | GO:0070626 | 0.04428 | Inf | 0.044 | 1 | 1 | (S)-2-(5-amino-1-(5-phospho-D-ribosyl)imidazole-4-carboxamido)succinate AMP-lyase (fumarate-forming) activity |
| GO: Molecular function | GO:0004408 | 0.04428 | Inf | 0.044 | 1 | 1 | holocytochrome-c synthase activity |
| GO: Molecular function | GO:0016796 | 0.04428 | Inf | 0.044 | 1 | 1 | exonuclease activity, active with either ribo- or deoxyribonucleic acids and producing 5’-phosphomonoesters |
| GO: Molecular function | GO:0070273 | 0.04428 | Inf | 0.044 | 1 | 1 | phosphatidylinositol-4-phosphate binding |
| GO: Cellular component | GO:0005802 | 0.00290 | Inf | 0.108 | 2 | 2 | trans-Golgi network |
| GO: Cellular component | GO:0008290 | 0.00290 | Inf | 0.108 | 2 | 2 | F-actin capping protein complex |
| GO: Cellular component | GO:0031984 | 0.02609 | 11.918 | 0.271 | 2 | 5 | organelle subcompartment |
Table S30: Results of KEGG and GO enrichment analysis for the genes in Module 6. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(6), gene.universe.modules,)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04140 | 0.00898 | 4.614 | 1.343 | 5 | 43 | Regulation of autophagy |
| KEGG | KEGG:03410 | 0.02970 | 9.357 | 0.281 | 2 | 9 | Base excision repair |
| GO: Biological process | GO:0007264 | 0.00057 | 4.722 | 2.539 | 9 | 62 | small GTPase mediated signal transduction |
| GO: Biological process | GO:0006913 | 0.00241 | 9.251 | 0.614 | 4 | 15 | nucleocytoplasmic transport |
| GO: Biological process | GO:0050789 | 0.00241 | 2.559 | 11.096 | 20 | 271 | regulation of biological process |
| GO: Biological process | GO:0000394 | 0.00479 | 48.977 | 0.123 | 2 | 3 | RNA splicing, via endonucleolytic cleavage and ligation |
| GO: Biological process | GO:0007165 | 0.00485 | 2.719 | 6.142 | 13 | 150 | signal transduction |
| GO: Biological process | GO:0023052 | 0.00614 | 2.631 | 6.306 | 13 | 154 | signaling |
| GO: Biological process | GO:0050896 | 0.00745 | 2.428 | 7.985 | 15 | 195 | response to stimulus |
| GO: Biological process | GO:0008033 | 0.03403 | 4.948 | 0.737 | 3 | 18 | tRNA processing |
| GO: Biological process | GO:0006420 | 0.04095 | Inf | 0.041 | 1 | 1 | arginyl-tRNA aminoacylation |
| GO: Biological process | GO:0000379 | 0.04095 | Inf | 0.041 | 1 | 1 | tRNA-type intron splice site recognition and cleavage |
| GO: Biological process | GO:0043086 | 0.04095 | Inf | 0.041 | 1 | 1 | negative regulation of catalytic activity |
| GO: Biological process | GO:0010923 | 0.04095 | Inf | 0.041 | 1 | 1 | negative regulation of phosphatase activity |
| GO: Biological process | GO:0045936 | 0.04095 | Inf | 0.041 | 1 | 1 | negative regulation of phosphate metabolic process |
| GO: Biological process | GO:0016559 | 0.04095 | Inf | 0.041 | 1 | 1 | peroxisome fission |
| GO: Biological process | GO:0048034 | 0.04095 | Inf | 0.041 | 1 | 1 | heme O biosynthetic process |
| GO: Biological process | GO:0000012 | 0.04095 | Inf | 0.041 | 1 | 1 | single strand break repair |
| GO: Biological process | GO:0051336 | 0.04095 | Inf | 0.041 | 1 | 1 | regulation of hydrolase activity |
| GO: Biological process | GO:0006384 | 0.04095 | Inf | 0.041 | 1 | 1 | transcription initiation from RNA polymerase III promoter |
| GO: Biological process | GO:0015031 | 0.04682 | 2.370 | 3.399 | 7 | 83 | protein transport |
| GO: Molecular function | GO:0019001 | 0.00049 | 4.645 | 2.429 | 9 | 66 | guanyl nucleotide binding |
| GO: Molecular function | GO:0005525 | 0.00049 | 4.645 | 2.429 | 9 | 66 | GTP binding |
| GO: Molecular function | GO:0003924 | 0.00084 | 6.561 | 1.178 | 6 | 32 | GTPase activity |
| GO: Molecular function | GO:0000213 | 0.00133 | Inf | 0.074 | 2 | 2 | tRNA-intron endonuclease activity |
| GO: Molecular function | GO:0016894 | 0.00391 | 54.000 | 0.110 | 2 | 3 | endonuclease activity, active with either ribo- or deoxyribonucleic acids and producing 3’-phosphomonoesters |
| GO: Molecular function | GO:0004521 | 0.01241 | 17.978 | 0.184 | 2 | 5 | endoribonuclease activity |
| GO: Molecular function | GO:0004518 | 0.01890 | 6.288 | 0.589 | 3 | 16 | nuclease activity |
| GO: Molecular function | GO:0004814 | 0.03680 | Inf | 0.037 | 1 | 1 | arginine-tRNA ligase activity |
| GO: Molecular function | GO:0008495 | 0.03680 | Inf | 0.037 | 1 | 1 | protoheme IX farnesyltransferase activity |
| GO: Molecular function | GO:0001106 | 0.03680 | Inf | 0.037 | 1 | 1 | RNA polymerase II transcription corepressor activity |
| GO: Molecular function | GO:0005488 | 0.04284 | 1.655 | 37.944 | 45 | 1031 | binding |
| GO: Molecular function | GO:0004842 | 0.04980 | 4.070 | 0.846 | 3 | 23 | ubiquitin-protein transferase activity |
| GO: Cellular component | GO:0044798 | 0.03728 | 8.314 | 0.318 | 2 | 8 | nuclear transcription factor complex |
| GO: Cellular component | GO:0000214 | 0.03977 | Inf | 0.040 | 1 | 1 | tRNA-intron endonuclease complex |
| GO: Cellular component | GO:0000126 | 0.03977 | Inf | 0.040 | 1 | 1 | transcription factor TFIIIB complex |
Table S31: Results of KEGG and GO enrichment analysis for the genes in Module 7. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(7), gene.universe.modules)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:04320 | 0.00313 | 14.022 | 0.321 | 3 | 10 | Dorso-ventral axis formation |
| KEGG | KEGG:04068 | 0.00434 | 7.427 | 0.707 | 4 | 22 | FoxO signaling pathway |
| KEGG | KEGG:00511 | 0.01389 | 15.909 | 0.193 | 2 | 6 | Other glycan degradation |
| KEGG | KEGG:04070 | 0.02071 | 6.082 | 0.611 | 3 | 19 | Phosphatidylinositol signaling system |
| KEGG | KEGG:00562 | 0.02720 | 5.396 | 0.675 | 3 | 21 | Inositol phosphate metabolism |
| GO: Biological process | GO:0007017 | 0.02023 | 6.159 | 0.606 | 3 | 18 | microtubule-based process |
| GO: Biological process | GO:0007165 | 0.02140 | 2.439 | 5.050 | 10 | 150 | signal transduction |
| GO: Biological process | GO:0022610 | 0.02348 | 5.768 | 0.640 | 3 | 19 | biological adhesion |
| GO: Biological process | GO:0023052 | 0.02543 | 2.361 | 5.185 | 10 | 154 | signaling |
| GO: Biological process | GO:0007156 | 0.02719 | 10.057 | 0.269 | 2 | 8 | homophilic cell adhesion via plasma membrane adhesion molecules |
| GO: Biological process | GO:0098609 | 0.02719 | 10.057 | 0.269 | 2 | 8 | cell-cell adhesion |
| GO: Biological process | GO:0034214 | 0.03367 | Inf | 0.034 | 1 | 1 | protein hexamerization |
| GO: Biological process | GO:0031117 | 0.03367 | Inf | 0.034 | 1 | 1 | positive regulation of microtubule depolymerization |
| GO: Biological process | GO:0043243 | 0.03367 | Inf | 0.034 | 1 | 1 | positive regulation of protein complex disassembly |
| GO: Molecular function | GO:0016887 | 0.00665 | 4.109 | 1.745 | 6 | 41 | ATPase activity |
| GO: Molecular function | GO:0016773 | 0.01212 | 2.708 | 3.830 | 9 | 90 | phosphotransferase activity, alcohol group as acceptor |
| GO: Molecular function | GO:0008270 | 0.01483 | 2.201 | 6.809 | 13 | 160 | zinc ion binding |
| GO: Molecular function | GO:0004553 | 0.02328 | 5.820 | 0.638 | 3 | 15 | hydrolase activity, hydrolyzing O-glycosyl compounds |
| GO: Molecular function | GO:0016301 | 0.02751 | 2.314 | 4.383 | 9 | 103 | kinase activity |
| GO: Molecular function | GO:0046872 | 0.03143 | 1.680 | 16.766 | 24 | 394 | metal ion binding |
| GO: Molecular function | GO:0045131 | 0.04255 | Inf | 0.043 | 1 | 1 | pre-mRNA branch point binding |
| GO: Molecular function | GO:0004565 | 0.04255 | Inf | 0.043 | 1 | 1 | beta-galactosidase activity |
| GO: Molecular function | GO:0008568 | 0.04255 | Inf | 0.043 | 1 | 1 | microtubule-severing ATPase activity |
| GO: Cellular component | GO:0090544 | 0.04772 | Inf | 0.048 | 1 | 1 | BAF-type complex |
| GO: Cellular component | GO:0030992 | 0.04772 | Inf | 0.048 | 1 | 1 | intraciliary transport particle B |
Table S32: Results of KEGG and GO enrichment analysis for the genes in Module 8. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(8), gene.universe.modules)
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:00190 | 0.000 | 390.754 | 1.305 | 26 | 49 | Oxidative phosphorylation |
| KEGG | KEGG:01100 | 0.000 | 66.522 | 9.107 | 28 | 342 | Metabolic pathways |
| GO: Biological process | GO:0009126 | 0.00000 | 87.347 | 0.300 | 8 | 22 | purine nucleoside monophosphate metabolic process |
| GO: Biological process | GO:0046034 | 0.00000 | 117.688 | 0.205 | 7 | 15 | ATP metabolic process |
| GO: Biological process | GO:0006163 | 0.00000 | 67.683 | 0.355 | 8 | 26 | purine nucleotide metabolic process |
| GO: Biological process | GO:0042278 | 0.00000 | 67.683 | 0.355 | 8 | 26 | purine nucleoside metabolic process |
| GO: Biological process | GO:0009161 | 0.00000 | 67.683 | 0.355 | 8 | 26 | ribonucleoside monophosphate metabolic process |
| GO: Biological process | GO:0009144 | 0.00000 | 85.352 | 0.246 | 7 | 18 | purine nucleoside triphosphate metabolic process |
| GO: Biological process | GO:0009259 | 0.00000 | 55.169 | 0.409 | 8 | 30 | ribonucleotide metabolic process |
| GO: Biological process | GO:0009119 | 0.00000 | 50.476 | 0.437 | 8 | 32 | ribonucleoside metabolic process |
| GO: Biological process | GO:0009199 | 0.00000 | 72.087 | 0.273 | 7 | 20 | ribonucleoside triphosphate metabolic process |
| GO: Biological process | GO:0015986 | 0.00000 | 541.500 | 0.082 | 5 | 6 | ATP synthesis coupled proton transport |
| GO: Biological process | GO:1901657 | 0.00000 | 48.411 | 0.450 | 8 | 33 | glycosyl compound metabolic process |
| GO: Biological process | GO:0009168 | 0.00000 | 89.667 | 0.191 | 6 | 14 | purine ribonucleoside monophosphate biosynthetic process |
| GO: Biological process | GO:0009206 | 0.00000 | 180.167 | 0.109 | 5 | 8 | purine ribonucleoside triphosphate biosynthetic process |
| GO: Biological process | GO:0046129 | 0.00000 | 71.600 | 0.218 | 6 | 16 | purine ribonucleoside biosynthetic process |
| GO: Biological process | GO:0009152 | 0.00000 | 65.030 | 0.232 | 6 | 17 | purine ribonucleotide biosynthetic process |
| GO: Biological process | GO:0009124 | 0.00000 | 54.923 | 0.259 | 6 | 19 | nucleoside monophosphate biosynthetic process |
| GO: Biological process | GO:0009142 | 0.00000 | 107.900 | 0.136 | 5 | 10 | nucleoside triphosphate biosynthetic process |
| GO: Biological process | GO:0072522 | 0.00000 | 50.952 | 0.273 | 6 | 20 | purine-containing compound biosynthetic process |
| GO: Biological process | GO:0006753 | 0.00000 | 26.387 | 0.723 | 8 | 53 | nucleoside phosphate metabolic process |
| GO: Biological process | GO:0009163 | 0.00000 | 44.500 | 0.300 | 6 | 22 | nucleoside biosynthetic process |
| GO: Biological process | GO:0046390 | 0.00000 | 44.500 | 0.300 | 6 | 22 | ribose phosphate biosynthetic process |
| GO: Biological process | GO:1902600 | 0.00000 | 76.929 | 0.164 | 5 | 12 | hydrogen ion transmembrane transport |
| GO: Biological process | GO:0098660 | 0.00000 | 76.929 | 0.164 | 5 | 12 | inorganic ion transmembrane transport |
| GO: Biological process | GO:0098655 | 0.00000 | 76.929 | 0.164 | 5 | 12 | cation transmembrane transport |
| GO: Biological process | GO:0006818 | 0.00000 | 67.250 | 0.177 | 5 | 13 | hydrogen transport |
| GO: Biological process | GO:0015672 | 0.00000 | 48.773 | 0.218 | 5 | 16 | monovalent inorganic cation transport |
| GO: Biological process | GO:0009165 | 0.00000 | 25.143 | 0.464 | 6 | 34 | nucleotide biosynthetic process |
| GO: Biological process | GO:0006793 | 0.00000 | 14.946 | 1.160 | 8 | 85 | phosphorus metabolic process |
| GO: Biological process | GO:0055085 | 0.00001 | 18.865 | 0.587 | 6 | 43 | transmembrane transport |
| GO: Biological process | GO:0044281 | 0.00002 | 10.456 | 1.979 | 9 | 145 | small molecule metabolic process |
| GO: Biological process | GO:0006811 | 0.00003 | 21.180 | 0.409 | 5 | 30 | ion transport |
| GO: Biological process | GO:0015980 | 0.00004 | 32.485 | 0.218 | 4 | 16 | energy derivation by oxidation of organic compounds |
| GO: Biological process | GO:1902578 | 0.00020 | 13.050 | 0.614 | 5 | 45 | single-organism localization |
| GO: Biological process | GO:0044711 | 0.00045 | 8.719 | 1.133 | 6 | 83 | single-organism biosynthetic process |
| GO: Biological process | GO:0042773 | 0.00052 | 166.615 | 0.041 | 2 | 3 | ATP synthesis coupled electron transport |
| GO: Biological process | GO:1901564 | 0.00138 | 5.740 | 2.566 | 8 | 188 | organonitrogen compound metabolic process |
| GO: Biological process | GO:0015991 | 0.00465 | 27.641 | 0.109 | 2 | 8 | ATP hydrolysis coupled proton transport |
| GO: Biological process | GO:0022904 | 0.01186 | Inf | 0.012 | 1 | 1 | respiratory electron transport chain |
| GO: Biological process | GO:0016310 | 0.01244 | 15.007 | 0.177 | 2 | 13 | phosphorylation |
| GO: Biological process | GO:0034244 | 0.01365 | Inf | 0.014 | 1 | 1 | negative regulation of transcription elongation from RNA polymerase II promoter |
| GO: Biological process | GO:0032784 | 0.01365 | Inf | 0.014 | 1 | 1 | regulation of DNA-templated transcription, elongation |
| GO: Biological process | GO:0006122 | 0.01365 | Inf | 0.014 | 1 | 1 | mitochondrial electron transport, ubiquinol to cytochrome c |
| GO: Biological process | GO:0051234 | 0.01424 | 3.752 | 2.894 | 7 | 212 | establishment of localization |
| GO: Biological process | GO:0006139 | 0.02489 | 3.325 | 4.058 | 8 | 318 | nucleobase-containing compound metabolic process |
| GO: Biological process | GO:0008152 | 0.02575 | 4.424 | 8.981 | 13 | 658 | metabolic process |
| GO: Biological process | GO:1902679 | 0.02712 | 77.357 | 0.027 | 1 | 2 | negative regulation of RNA biosynthetic process |
| GO: Biological process | GO:0044208 | 0.02712 | 77.357 | 0.027 | 1 | 2 | ‘de novo’ AMP biosynthetic process |
| GO: Biological process | GO:0045934 | 0.02712 | 77.357 | 0.027 | 1 | 2 | negative regulation of nucleobase-containing compound metabolic process |
| GO: Biological process | GO:0009890 | 0.02712 | 77.357 | 0.027 | 1 | 2 | negative regulation of biosynthetic process |
| GO: Biological process | GO:0045892 | 0.02712 | 77.357 | 0.027 | 1 | 2 | negative regulation of transcription, DNA-templated |
| GO: Biological process | GO:0010605 | 0.02712 | 77.357 | 0.027 | 1 | 2 | negative regulation of macromolecule metabolic process |
| GO: Biological process | GO:0022900 | 0.03255 | 49.136 | 0.033 | 1 | 3 | electron transport chain |
| GO: Biological process | GO:0055114 | 0.03654 | 39.556 | 0.037 | 1 | 4 | oxidation-reduction process |
| GO: Molecular function | GO:0046933 | 0.00000 | Inf | 0.072 | 5 | 5 | proton-transporting ATP synthase activity, rotational mechanism |
| GO: Molecular function | GO:0015077 | 0.00000 | 44.340 | 0.374 | 8 | 26 | monovalent inorganic cation transmembrane transporter activity |
| GO: Molecular function | GO:0008324 | 0.00000 | 20.211 | 0.676 | 8 | 47 | cation transmembrane transporter activity |
| GO: Molecular function | GO:0042625 | 0.00000 | 71.167 | 0.158 | 5 | 11 | ATPase coupled ion transmembrane transporter activity |
| GO: Molecular function | GO:0022891 | 0.00000 | 15.243 | 1.006 | 9 | 70 | substrate-specific transmembrane transporter activity |
| GO: Molecular function | GO:0008137 | 0.00000 | 163.048 | 0.086 | 4 | 6 | NADH dehydrogenase (ubiquinone) activity |
| GO: Molecular function | GO:0016655 | 0.00000 | 163.048 | 0.086 | 4 | 6 | oxidoreductase activity, acting on NAD(P)H, quinone or similar compound as acceptor |
| GO: Molecular function | GO:0003954 | 0.00000 | 163.048 | 0.086 | 4 | 6 | NADH dehydrogenase activity |
| GO: Molecular function | GO:0015405 | 0.00000 | 42.600 | 0.216 | 5 | 15 | P-P-bond-hydrolysis-driven transmembrane transporter activity |
| GO: Molecular function | GO:0005215 | 0.00000 | 10.536 | 1.610 | 10 | 112 | transporter activity |
| GO: Molecular function | GO:0016820 | 0.00000 | 35.458 | 0.244 | 5 | 17 | hydrolase activity, acting on acid anhydrides, catalyzing transmembrane movement of substances |
| GO: Molecular function | GO:0043492 | 0.00000 | 35.458 | 0.244 | 5 | 17 | ATPase activity, coupled to movement of substances |
| GO: Molecular function | GO:0046961 | 0.00003 | 116.727 | 0.072 | 3 | 5 | proton-transporting ATPase activity, rotational mechanism |
| GO: Molecular function | GO:0009055 | 0.00007 | 64.088 | 0.093 | 3 | 7 | electron carrier activity |
| GO: Molecular function | GO:0016887 | 0.00021 | 11.653 | 0.589 | 5 | 41 | ATPase activity |
| GO: Molecular function | GO:0016675 | 0.00059 | 148.957 | 0.043 | 2 | 3 | oxidoreductase activity, acting on a heme group of donors |
| GO: Molecular function | GO:0004129 | 0.00059 | 148.957 | 0.043 | 2 | 3 | cytochrome-c oxidase activity |
| GO: Molecular function | GO:0051540 | 0.00107 | 19.341 | 0.216 | 3 | 15 | metal cluster binding |
| GO: Molecular function | GO:0003824 | 0.00165 | 4.531 | 13.528 | 21 | 941 | catalytic activity |
| GO: Molecular function | GO:0016651 | 0.00283 | 35.937 | 0.085 | 2 | 7 | oxidoreductase activity, acting on NAD(P)H |
| GO: Molecular function | GO:0051539 | 0.00399 | 29.722 | 0.101 | 2 | 7 | 4 iron, 4 sulfur cluster binding |
| GO: Molecular function | GO:0008121 | 0.01438 | Inf | 0.014 | 1 | 1 | ubiquinol-cytochrome-c reductase activity |
| GO: Molecular function | GO:0004019 | 0.01438 | Inf | 0.014 | 1 | 1 | adenylosuccinate synthase activity |
| GO: Molecular function | GO:0032450 | 0.01438 | Inf | 0.014 | 1 | 1 | maltose alpha-glucosidase activity |
| GO: Molecular function | GO:0015926 | 0.01438 | Inf | 0.014 | 1 | 1 | glucosidase activity |
| GO: Molecular function | GO:0016679 | 0.01438 | Inf | 0.014 | 1 | 1 | oxidoreductase activity, acting on diphenols and related substances as donors |
| GO: Molecular function | GO:0004558 | 0.01438 | Inf | 0.014 | 1 | 1 | alpha-1,4-glucosidase activity |
| GO: Molecular function | GO:0010181 | 0.01438 | Inf | 0.014 | 1 | 1 | FMN binding |
| GO: Molecular function | GO:0020037 | 0.01625 | 12.333 | 0.201 | 2 | 14 | heme binding |
| GO: Molecular function | GO:0016462 | 0.02190 | 3.610 | 1.668 | 5 | 116 | pyrophosphatase activity |
| GO: Molecular function | GO:0004784 | 0.02855 | 71.375 | 0.029 | 1 | 2 | superoxide dismutase activity |
| GO: Molecular function | GO:0000104 | 0.02855 | 71.375 | 0.029 | 1 | 2 | succinate dehydrogenase activity |
| GO: Molecular function | GO:0008308 | 0.04254 | 35.667 | 0.043 | 1 | 3 | voltage-gated anion channel activity |
| GO: Cellular component | GO:0031975 | 0.00000 | 43.071 | 0.482 | 9 | 29 | envelope |
| GO: Cellular component | GO:0005740 | 0.00000 | 54.898 | 0.350 | 8 | 22 | mitochondrial envelope |
| GO: Cellular component | GO:0005743 | 0.00000 | 65.674 | 0.266 | 7 | 16 | mitochondrial inner membrane |
| GO: Cellular component | GO:0045261 | 0.00000 | Inf | 0.067 | 4 | 4 | proton-transporting ATP synthase complex, catalytic core F(1) |
| GO: Cellular component | GO:0031090 | 0.00000 | 21.446 | 0.682 | 8 | 41 | organelle membrane |
| GO: Cellular component | GO:0005739 | 0.00000 | 20.338 | 0.610 | 7 | 42 | mitochondrion |
| GO: Cellular component | GO:0098803 | 0.00000 | Inf | 0.048 | 3 | 3 | respiratory chain complex |
| GO: Cellular component | GO:0016469 | 0.00003 | 35.579 | 0.200 | 4 | 12 | proton-transporting two-sector ATPase complex |
| GO: Cellular component | GO:0098798 | 0.00008 | 67.850 | 0.100 | 3 | 6 | mitochondrial protein complex |
| GO: Cellular component | GO:0044455 | 0.00008 | 67.850 | 0.100 | 3 | 6 | mitochondrial membrane part |
| GO: Cellular component | GO:0070469 | 0.00018 | Inf | 0.028 | 2 | 2 | respiratory chain |
| GO: Cellular component | GO:0070069 | 0.00026 | Inf | 0.033 | 2 | 2 | cytochrome complex |
| GO: Cellular component | GO:0044446 | 0.00049 | 4.947 | 3.210 | 10 | 193 | intracellular organelle part |
| GO: Cellular component | GO:0005737 | 0.01340 | 2.901 | 4.906 | 10 | 295 | cytoplasm |
| GO: Cellular component | GO:0044425 | 0.01400 | 3.663 | 8.055 | 13 | 651 | membrane part |
| GO: Cellular component | GO:0005750 | 0.01663 | Inf | 0.017 | 1 | 1 | mitochondrial respiratory chain complex III |
| GO: Cellular component | GO:0005751 | 0.01663 | Inf | 0.017 | 1 | 1 | mitochondrial respiratory chain complex IV |
| GO: Cellular component | GO:0005747 | 0.01663 | Inf | 0.017 | 1 | 1 | mitochondrial respiratory chain complex I |
| GO: Cellular component | GO:0045281 | 0.01663 | Inf | 0.017 | 1 | 1 | succinate dehydrogenase complex |
| GO: Cellular component | GO:0030964 | 0.01663 | Inf | 0.017 | 1 | 1 | NADH dehydrogenase complex |
| GO: Cellular component | GO:0032021 | 0.01663 | Inf | 0.017 | 1 | 1 | NELF complex |
| GO: Cellular component | GO:0005758 | 0.03300 | 61.773 | 0.033 | 1 | 2 | mitochondrial intermembrane space |
| GO: Cellular component | GO:0032991 | 0.03576 | 2.457 | 4.839 | 9 | 291 | macromolecular complex |
| GO: Cellular component | GO:0005741 | 0.04910 | 30.864 | 0.050 | 1 | 3 | mitochondrial outer membrane |
Table S33: Results of KEGG and GO enrichment analysis for the genes in Module 9. The gene universe was defined as all genes for which we found an ortholog in all four species.
GO.and.KEGG.enrichment(genes.in.module(9), gene.universe.modules)
## Warning: No results met the specified criteria. Returning 0-row data.frame
| Test_type | ID | Pvalue | OddsRatio | ExpCount | Count | Size | Term |
|---|---|---|---|---|---|---|---|
| KEGG | KEGG:00230 | 0.00825 | 9.885 | 0.455 | 3 | 55 | Purine metabolism |
| KEGG | KEGG:00430 | 0.01647 | 134.875 | 0.017 | 1 | 2 | Taurine and hypotaurine metabolism |
| KEGG | KEGG:00981 | 0.04868 | 26.875 | 0.050 | 1 | 6 | Insect hormone biosynthesis |
| GO: Biological process | GO:0006275 | 0.01632 | 136.125 | 0.016 | 1 | 2 | regulation of DNA replication |
| GO: Biological process | GO:0035556 | 0.03782 | 5.298 | 0.794 | 3 | 97 | intracellular signal transduction |
| GO: Molecular function | GO:0004383 | 0.00067 | 101.059 | 0.044 | 2 | 4 | guanylate cyclase activity |
| GO: Molecular function | GO:0016829 | 0.00581 | 9.891 | 0.382 | 3 | 35 | lyase activity |
| GO: Molecular function | GO:0020037 | 0.00952 | 16.745 | 0.153 | 2 | 14 | heme binding |
| GO: Molecular function | GO:0004045 | 0.01093 | Inf | 0.011 | 1 | 1 | aminoacyl-tRNA hydrolase activity |
| GO: Molecular function | GO:0004000 | 0.01093 | Inf | 0.011 | 1 | 1 | adenosine deaminase activity |
| GO: Molecular function | GO:0030337 | 0.01093 | Inf | 0.011 | 1 | 1 | DNA polymerase processivity factor activity |
| GO: Molecular function | GO:0016702 | 0.02174 | 95.500 | 0.022 | 1 | 2 | oxidoreductase activity, acting on single donors with incorporation of molecular oxygen, incorporation of two atoms of oxygen |
| GO: Molecular function | GO:1901363 | 0.03930 | 2.528 | 7.725 | 12 | 707 | heterocyclic compound binding |
| GO: Molecular function | GO:0097159 | 0.03930 | 2.528 | 7.725 | 12 | 707 | organic cyclic compound binding |
| GO: Molecular function | GO:0004672 | 0.04241 | 4.420 | 0.798 | 3 | 73 | protein kinase activity |
| GO: Molecular function | GO:0004715 | 0.04303 | 31.796 | 0.044 | 1 | 4 | non-membrane spanning protein tyrosine kinase activity |
Table S34: List of all the genes in Module 4, ranked by their within-module connectivity, k. The latter four columns give the Log\(_2\) fold-change in expression in response to queen pheromone in each of the four species.
inspect.module.genes(4) %>%
mutate(am_fc=log2(am_fc), bt_fc=log2(bt_fc), lf_fc=log2(lf_fc), ln_fc=log2(ln_fc)) %>%
rename(Gene=gene, Name=name) %>%
kable.table()
| Gene | Name | k | am_fc | bt_fc | lf_fc | ln_fc |
|---|---|---|---|---|---|---|
| GB44431 | 26S protease regulatory subunit 4 isoform 1 | 44.223556 | 0.2068368 | -0.0420157 | -0.4280960 | -0.0088204 |
| GB49337 | 26S proteasome non-ATPase regulatory subunit 13 | 42.984225 | 0.1764581 | -0.0655698 | -0.2607125 | -0.5605728 |
| GB50750 | coatomer subunit delta isoform 2 | 42.890303 | -0.0312791 | -0.0288217 | -0.0588197 | -0.0489833 |
| GB45720 | proteasome subunit alpha type-7-1-like | 41.581027 | 0.1530987 | -0.0949419 | -0.0722067 | 0.0630901 |
| GB50242 | 26S proteasome non-ATPase regulatory subunit 4 | 41.384303 | 0.2213651 | 0.0631539 | -0.1328648 | 0.5944635 |
| GB53174 | programmed cell death 6-interacting protein isoform X1 | 41.242520 | -0.0756447 | -0.0159918 | -0.0466398 | -0.0545396 |
| GB47189 | H(+)/Cl(-) exchange transporter 3-like isoform X2 | 41.034107 | 0.0346407 | -0.0154327 | -0.1018644 | -0.0454175 |
| GB50252 | GTP-binding protein SAR1b-like isoform X4 | 40.648326 | 0.3208936 | -0.0667845 | -0.0210473 | -0.2223932 |
| 102656372 | tropinone reductase 2-like | 39.868937 | 0.1120373 | 0.0340800 | 0.3238888 | 0.4926542 |
| GB53812 | prolyl endopeptidase-like isoformX1 | 39.532524 | -0.0804557 | -0.0489813 | -0.0926730 | -0.0238204 |
| GB45567 | E3 ubiquitin-protein ligase MARCH5 isoform X5 | 39.470727 | -0.0551062 | 0.0346992 | 0.4749971 | 0.0134325 |
| GB41649 | E3 ubiquitin-protein ligase MARCH6 | 39.278828 | -0.0462292 | -0.0638063 | -0.0682451 | 0.0497685 |
| GB43819 | ATPase ASNA1 homolog | 39.180343 | 0.3773737 | -0.0065874 | -0.1431066 | -0.0100659 |
| GB44941 | eukaryotic peptide chain release factor GTP-binding subunit ERF3A | 39.104220 | -0.0593707 | 0.0722754 | -0.0148940 | -0.1104174 |
| GB53690 | protein transport protein Sec31A | 38.707647 | -0.0073805 | 0.0306890 | -0.1181363 | -0.0320893 |
| GB48643 | STT3, subunit of the oligosaccharyltransferase complex, homolog B | 37.962742 | 0.1934304 | 0.0005876 | -0.1604664 | -0.0954778 |
| GB50348 | bleomycin hydrolase-like isoform X2 | 37.858985 | -0.0331317 | 0.0361318 | -0.0548069 | 0.0615163 |
| GB43706 | probable trans-2-enoyl-CoA reductase, mitochondrial-like | 37.473883 | -0.0105284 | 0.0051152 | -0.0134324 | 0.0351066 |
| GB40775 | apoptosis-inducing factor 1, mitochondrial | 36.869445 | 0.2000561 | 0.1909935 | 0.3170325 | 0.0325652 |
| 411789 | protein extra bases | 36.857043 | 0.1887237 | 0.0207032 | -0.1285144 | 0.1008955 |
| GB40483 | xyloside xylosyltransferase 1-like | 36.852931 | 0.0301872 | 0.0061033 | -0.0806551 | 0.0684976 |
| GB41617 | methylcrotonoyl-CoA carboxylase beta chain, mitochondrial-like isoform X2 | 36.788246 | 0.1487599 | -0.1687086 | -0.2389065 | -0.0591055 |
| GB50289 | signal recognition particle 54 kDa protein-like | 36.640755 | 0.0039203 | -0.0010764 | -0.0138630 | -0.0199337 |
| GB50274 | transitional endoplasmic reticulum ATPase TER94 | 36.259304 | 0.5435617 | -0.1180270 | -0.3064504 | -0.0779525 |
| GB47540 | putative leucine-rich repeat-containing protein DDB_G0290503 isoform X2 | 36.214750 | 0.2775390 | 0.0232034 | -0.1293343 | 0.0217957 |
| GB47573 | T-complex protein 1 subunit theta-like | 36.082403 | 0.1562527 | 0.0513066 | -0.0207824 | -0.0623897 |
| GB52675 | 26S proteasome non-ATPase regulatory subunit 12 | 35.929513 | 0.2312931 | 0.0482900 | -0.0951427 | 0.7829533 |
| GB42355 | asparagine–tRNA ligase, cytoplasmic-like | 35.911929 | 0.1286098 | 0.1015732 | -0.1220399 | -0.0430047 |
| GB42329 | segmentation protein cap’n’collar-like isoform X4 | 35.867197 | -0.2192666 | -0.1006952 | -0.1213930 | 0.6014040 |
| GB55494 | probable nucleolar GTP-binding protein 1-like isoform 1 | 35.759099 | 0.0447120 | 0.0957711 | 3.8215256 | -0.1220854 |
| GB42773 | alanine–tRNA ligase, cytoplasmic-like isoform X1 | 35.229118 | -0.0350767 | 0.0415367 | -0.0868974 | 0.0119881 |
| GB50730 | 97 kDa heat shock protein isoformX1 | 35.063680 | -0.1577197 | -0.0288468 | -0.2107992 | -0.1611854 |
| GB48313 | transmembrane 9 superfamily member 3 | 34.685061 | 0.2534914 | -0.0136668 | -0.0312486 | -0.0353920 |
| GB50459 | WD repeat-containing protein 36-like | 34.578669 | -0.1479411 | -0.0430390 | -0.2433271 | -0.1232282 |
| GB46035 | eukaryotic translation initiation factor 4 gamma 2-like isoform X4 | 33.921974 | -0.2214407 | 0.0295406 | -0.2425567 | -0.1486897 |
| GB54608 | probable elongator complex protein 2-like | 33.814252 | 0.0689425 | 0.0691345 | -0.2205388 | -0.1308013 |
| GB50177 | protein TRC8 homolog | 33.492549 | 0.0945129 | 0.1231066 | -0.1733043 | 0.2465639 |
| GB45258 | isocitrate dehydrogenase [NADP] cytoplasmic isoform 2 | 33.420505 | -0.0142164 | -0.0157218 | -0.1189860 | -0.0987758 |
| GB47114 | dolichyl-diphosphooligosaccharide–protein glycosyltransferase subunit 2-like | 33.136515 | 0.1350366 | 0.1040145 | -0.1152653 | -0.1108689 |
| GB44418 | protein suppressor of hairy wing isoform X2 | 33.079975 | -0.4107368 | -0.1260784 | -0.2722544 | 0.0277971 |
| GB54573 | probable 26S proteasome non-ATPase regulatory subunit 3 isoform X2 | 31.928635 | 0.0538327 | -0.0037021 | -0.0681125 | -0.9049955 |
| GB55440 | phosphatidylinositol transfer protein alpha isoform | 31.910100 | 0.1654650 | 0.0068526 | -0.0463461 | 0.0630027 |
| GB41762 | derlin-2-like | 31.704673 | 0.1842082 | 0.0872893 | -0.2212623 | -0.1243794 |
| GB49939 | protein FAM188A homolog | 31.551690 | -0.1412746 | 0.1136928 | -0.1907462 | 0.0388591 |
| GB42648 | dolichyl-diphosphooligosaccharide–protein glycosyltransferase subunit 1 | 31.480759 | 0.2655380 | 0.1595473 | -0.1227576 | -0.1662744 |
| GB44670 | luciferin 4-monooxygenase-like | 31.430736 | -0.0515925 | 0.1548945 | 1.1032901 | 0.0559438 |
| GB43131 | short-chain dehydrogenase/reductase family 16C member 6-like isoform X4 | 31.410234 | 0.1007306 | 0.0869099 | -0.1985410 | -0.0829191 |
| GB48692 | translocation protein SEC63 homolog isoform 1 | 31.125908 | 0.2857900 | -0.0530291 | -0.1602624 | 0.0209032 |
| GB49083 | casein kinase II subunit beta isoform X1 | 30.992393 | 0.2782502 | 0.0471649 | -0.1111348 | 0.0698090 |
| GB41427 | catalase | 30.732896 | 0.1430821 | 0.0736901 | -0.3977072 | -0.0121187 |
| GB46735 | eukaryotic translation initiation factor 2A-like | 30.705422 | -0.0411662 | 0.0130254 | -0.1447461 | -0.0105182 |
| GB47296 | transmembrane protein 19-like isoform X2 | 30.672830 | 0.4289691 | -0.0545500 | -0.2516466 | -0.1027988 |
| GB52168 | von Willebrand factor A domain-containing protein 8-like | 30.577444 | 0.0856555 | -0.0740676 | 0.0014012 | 0.0699640 |
| GB48812 | dnaJ homolog subfamily C member 3 | 30.546137 | 0.1132367 | 0.0402074 | -0.2195332 | 0.0306329 |
| 102655967 | ancient ubiquitous protein 1-like | 30.348262 | 0.4711330 | 0.0420199 | 0.1648789 | 0.0503451 |
| 551499 | FIT family protein CG10671-like | 29.740675 | 0.3785333 | -0.0602509 | -0.3180826 | -0.0349339 |
| GB49955 | vacuole membrane protein 1 isoform X1 | 29.459325 | -0.0443525 | -0.0065202 | -0.2963167 | 0.1983572 |
| GB41285 | receptor-binding cancer antigen expressed on SiSo cells | 29.433269 | 0.0238298 | 0.1200911 | -0.1399244 | -0.1309690 |
| GB54861 | LOW QUALITY PROTEIN: counting factor associated protein D-like | 29.320266 | 0.2298241 | 0.1926641 | -0.2944184 | -0.0974716 |
| GB47462 | protein disulfide-isomerase A3 isoform 2 | 29.268674 | 0.3049034 | 0.0771835 | -0.2557549 | 0.1369471 |
| GB46646 | UPF0554 protein C2orf43 homolog | 28.707580 | 0.3354412 | -0.0495704 | -0.2178741 | -0.1430792 |
| GB44396 | atlastin isoform X2 | 28.556709 | -0.0591485 | -0.1777902 | -0.0925969 | 0.3200035 |
| GB53373 | leucine-rich repeat-containing protein 58-like | 28.367576 | 0.1837683 | 0.0574237 | -0.2601640 | 0.1579574 |
| GB55484 | UBX domain-containing protein 7-like | 28.345099 | -0.1419776 | 0.0862990 | -0.1770521 | -0.0476737 |
| GB47134 | renin receptor-like isoform X1 | 28.303254 | 0.3303687 | -0.0407767 | 0.3718194 | 0.4166502 |
| GB43912 | nicalin-1 isoform X1 | 28.248461 | 0.6287100 | 0.0881076 | -0.3253488 | -0.0103644 |
| GB46120 | aspartate aminotransferase, mitochondrial isoform 1 | 28.225409 | 0.2491141 | 0.0236496 | 0.1306639 | 0.0254197 |
| GB49525 | RNA-binding protein fusilli | 28.209030 | 0.1174438 | -0.0741709 | -0.0349456 | 0.0534866 |
| GB48597 | NADH-cytochrome b5 reductase 2-like isoform X2 | 28.155088 | 0.2033803 | 0.0013862 | -0.0996939 | -0.0202651 |
| GB44205 | proteasome subunit beta type-5-like | 28.006936 | 0.4837999 | -0.0915736 | -0.4335090 | -0.0596112 |
| GB52434 | probable ribosome production factor 1-like | 27.874103 | 0.0054318 | 0.0148853 | -0.2060277 | 0.0182433 |
| GB40779 | transaldolase | 27.760521 | -0.0039251 | 0.0160977 | -0.0440904 | 0.0344095 |
| GB45582 | facilitated trehalose transporter Tret1-like isoform 3 | 27.374644 | -0.0504268 | -0.1335269 | 0.0539026 | -0.0069750 |
| GB45698 | SAGA-associated factor 11 homolog | 27.343826 | -0.2647791 | 0.0924924 | -0.1384764 | 0.1879171 |
| GB40265 | transcriptional activator protein Pur-beta-B-like isoform X4 | 27.334314 | 0.1264999 | -0.0386187 | -0.1285937 | -0.0782933 |
| GB47392 | protein BCCIP homolog | 27.258892 | 0.2577727 | 0.1104351 | 0.7443079 | 0.1332378 |
| GB55987 | ras-related protein Rab-18-B | 27.110725 | 0.0323400 | -0.0536913 | -0.0349277 | -0.0504278 |
| GB55977 | eukaryotic translation initiation factor 4E-1A | 27.089946 | 0.1705188 | 0.0538447 | -0.0949449 | 0.1031615 |
| GB45251 | ubiA prenyltransferase domain-containing protein 1 homolog | 26.995162 | 0.2292889 | 0.0114163 | -0.1159756 | 0.0793336 |
| GB48008 | peroxisomal membrane protein PEX14-like | 26.969623 | 0.0001390 | 0.0224702 | -0.2071820 | -0.0800297 |
| GB46977 | ribosome biogenesis methyltransferase WBSCR22-like | 26.952365 | 0.0481658 | 0.0896746 | -0.2062109 | 0.0893196 |
| GB54363 | ATPase family AAA domain-containing protein 3 isoform X1 | 26.942276 | 0.3943176 | 0.1631272 | -0.1500874 | -0.0561398 |
| GB53955 | FGFR1 oncogene partner 2 homolog | 26.809933 | 0.0846268 | -0.0312388 | -0.1442031 | 0.0964404 |
| GB51282 | thioredoxin domain-containing protein 5-like isoform 1 | 26.691792 | 0.2485396 | 0.0763851 | 0.1463655 | -0.0113567 |
| GB46031 | vacuolar H+ ATP synthase 16 kDa proteolipid subunit | 26.645728 | -0.0479109 | -0.0170686 | -0.2826372 | 0.0222715 |
| GB54848 | tumor suppressor candidate 3-like | 26.523213 | 0.4846324 | -0.0104631 | -0.6272344 | -0.0006124 |
| GB49119 | deoxynucleotidyltransferase terminal-interacting protein 2-like | 26.458317 | 0.2109767 | -0.0144902 | -0.1065953 | 0.0599639 |
| GB53080 | alpha-2-macroglobulin receptor-associated protein-like | 26.455789 | 0.0064170 | -0.0306365 | -0.0869340 | 0.0369668 |
| GB49117 | heat shock protein cognate 3 precursor | 26.360858 | 0.2270221 | -0.0395375 | -0.2932567 | -0.1580736 |
| GB49240 | aldehyde dehydrogenase, mitochondrial isoform 1 | 26.349079 | 0.1549590 | 0.1010275 | -0.0376052 | -0.0094109 |
| GB55610 | MOSC domain-containing protein 2, mitochondrial-like | 26.339169 | -0.0627471 | 0.0072092 | 0.3240534 | -0.1399329 |
| GB49307 | DNA-directed RNA polymerases I and III subunit RPAC1-like isoform X1 | 26.293649 | -0.0115285 | 0.0668726 | 0.3393313 | -0.0367022 |
| GB52729 | aspartate–tRNA ligase, cytoplasmic | 26.270157 | 0.1271826 | -0.0104019 | 7.4806151 | -0.0363266 |
| GB40207 | serine–tRNA ligase, mitochondrial | 26.269427 | 0.0012962 | -0.0721504 | 0.0021323 | -0.0446679 |
| GB46979 | derlin-1-like | 26.162259 | 0.6809454 | -0.0344909 | 0.5101016 | -0.0139263 |
| GB42236 | patched domain-containing protein 3-like isoform X4 | 25.938301 | -0.2888681 | 0.0901237 | -0.1149775 | 0.1142936 |
| 102653839 | histone-lysine N-methyltransferase SETMAR-like | 25.496262 | 0.2063172 | -0.0636157 | -0.2265030 | -0.1742015 |
| GB49180 | cysteine-rich secretory protein 1-like, transcript variant X5 | 25.371025 | -0.2540170 | -0.0393153 | -0.1190649 | -0.2517126 |
| GB55537 | transketolase isoform 1 | 25.321298 | 1.0357857 | 0.0369899 | -0.2479617 | -0.3417730 |
| GB54999 | NAD kinase 2, mitochondrial-like | 25.209366 | 0.4540230 | -0.2140000 | -0.0815604 | -0.0922070 |
| GB54101 | HEAT repeat-containing protein 3-like | 24.883603 | -0.2253708 | -0.0872323 | -0.1050610 | 0.0597797 |
| GB55490 | uncharacterized protein LOC410793 | 24.753469 | -0.0477751 | -0.0681408 | -0.4730765 | 0.2615252 |
| GB46579 | glucose-6-phosphate 1-dehydrogenase isoform X3 | 24.688398 | 0.6482683 | -0.1000294 | -0.3650464 | -0.1593256 |
| GB50096 | pantothenate kinase 1-like isoform X2 | 24.586554 | 0.8477323 | -0.0870535 | -0.3693640 | -0.0267439 |
| GB54112 | adenine phosphoribosyltransferase isoform X1 | 24.536162 | 0.2345084 | 0.0448087 | 1.4763523 | 0.1039490 |
| GB47432 | 5-aminolevulinate synthase, erythroid-specific, mitochondrial-like | 24.361288 | 0.3065397 | -0.2485980 | -0.3612845 | -0.0388571 |
| GB40783 | glucose-6-phosphate isomerase-like | 24.207603 | -0.2439304 | -0.1024763 | -0.0910389 | -0.0013179 |
| GB54298 | stromal cell-derived factor 2-like protein 1-like isoformX2 | 24.138324 | 0.3180715 | 0.0516537 | -0.2166825 | 1.5192543 |
| GB44457 | FGGY carbohydrate kinase domain-containing protein-like isoform X2 | 23.955079 | 0.3022943 | -0.1605569 | -0.2354506 | -0.0710812 |
| GB48408 | protein catecholamines up | 23.947718 | 0.0141547 | -0.0116125 | -0.1088589 | 0.0730103 |
| GB48847 | DNA replication licensing factor Mcm3 | 23.786913 | -0.3084852 | 0.2500155 | -0.2998054 | 0.1204342 |
| GB46657 | galactokinase-like | 23.579329 | 0.1002480 | 0.0684625 | -0.5178679 | 0.0198896 |
| GB52347 | saccharopine dehydrogenase-like oxidoreductase-like isoform 1 | 23.401023 | 0.3645361 | -0.4951154 | 0.2533578 | -0.1998256 |
| GB51782 | carboxypeptidase Q-like isoform 1 | 23.387758 | 0.3346236 | -0.0203412 | -0.0649589 | -0.1664672 |
| GB48308 | probable pyruvate dehydrogenase E1 component subunit alpha, mitochondrial-like isoform X2 | 23.311737 | -0.2837578 | -0.1078497 | 0.1711523 | 0.5184012 |
| GB44557 | probable ribonuclease ZC3H12C-like isoformX1 | 23.279307 | 0.0744929 | -0.0447778 | -0.1440084 | -0.3265611 |
| GB47941 | cyclic AMP response element-binding protein A-like | 23.225979 | -0.3397125 | 0.1288849 | -0.1450569 | -0.3071147 |
| GB42732 | long-chain-fatty-acid–CoA ligase 3-like isoform X2 | 23.218782 | 0.4989058 | -0.0146724 | -0.3252347 | -0.1571386 |
| GB52724 | protein 5NUC-like isoform X2 | 23.028043 | 0.0972367 | 0.0206395 | -0.1179516 | 0.0023551 |
| GB46772 | very-long-chain enoyl-CoA reductase-like | 23.018130 | 0.7467499 | -0.2199431 | -0.2011022 | -0.4308688 |
| GB44008 | BTB/POZ domain-containing protein 17 isoform X1 | 22.839645 | 0.3154921 | 0.1167502 | -0.1116056 | -0.0483891 |
| GB55511 | growth/differentiation factor 8-like isoform 1 | 22.816925 | 0.4352292 | 0.1588802 | -0.4870545 | 0.0743345 |
| GB54601 | protein disulfide-isomerase A6-like isoform 1 | 22.775763 | 0.4324571 | 0.1249594 | -0.1467693 | -0.0779340 |
| GB49342 | sugar phosphate exchanger 2-like isoform X3 | 22.718190 | -0.2236853 | -0.0107231 | -0.0067022 | 0.0247381 |
| GB49348 | transmembrane protein 115-like | 22.714857 | 0.3394745 | -0.0382297 | -0.0306424 | -0.0288120 |
| GB41388 | glycerol-3-phosphate dehydrogenase | 22.668744 | -0.0851797 | -0.1391961 | -0.1883058 | 0.2562985 |
| GB49336 | acetyl-CoA carboxylase-like isoform X9 | 22.667437 | 0.3952476 | -0.1602047 | 0.1869465 | -0.2268771 |
| GB54056 | serine hydroxymethyltransferase, cytosolic isoform X3 | 22.549057 | 0.4140579 | 0.1933755 | -0.3256797 | -0.2607203 |
| GB44640 | solute carrier family 52, riboflavin transporter, member 3-A-like isoform X2 | 22.453147 | -0.1275523 | -0.1027834 | 0.1884364 | -0.2170403 |
| GB49826 | sterol O-acyltransferase 1-like | 22.192329 | 0.0951372 | 0.1465247 | -0.2836459 | 0.0229186 |
| GB47694 | globin 1 | 22.014317 | -0.0509277 | 0.1091362 | -0.1515248 | -0.1010404 |
| GB52074 | 6-phosphogluconate dehydrogenase, decarboxylating | 21.966722 | 0.8095794 | -0.1426001 | -0.4446501 | -0.6031632 |
| GB48195 | acyl-CoA Delta(11) desaturase-like | 21.937703 | 0.4943072 | -0.1931849 | 0.6995588 | 0.6686102 |
| GB45213 | acyl-CoA synthetase short-chain family member 3, mitochondrial-like isoform X2 | 21.833726 | 0.6513876 | 0.2239474 | -0.5637999 | -0.2397701 |
| GB50680 | mannose-P-dolichol utilization defect 1 protein homolog isoform X2 | 21.555807 | 0.4656771 | -0.3933720 | -0.2207091 | -0.0486393 |
| GB45775 | pancreatic triacylglycerol lipase-like isoform X2 | 21.506443 | 0.3197015 | 0.0505266 | -0.8880584 | 0.0691686 |
| GB41916 | uncharacterized protein LOC726658 isoform 1 | 21.370720 | 0.3361149 | 0.3728404 | -0.0276391 | -0.0165127 |
| GB52458 | cysteine-rich with EGF-like domain protein 2-like | 21.264629 | -0.2710389 | 0.0498794 | -0.3606772 | -0.0178730 |
| GB40278 | probable methylmalonate-semialdehyde dehydrogenase [acylating], mitochondrial isoform X4 | 21.241766 | -0.1582318 | 0.0029943 | 0.0294265 | -0.0342272 |
| GB54216 | ATP-citrate synthase isoform X2 | 21.223912 | 0.8455868 | -0.2267974 | -0.4457293 | -0.3264580 |
| 552211 | protein THEM6-like | 21.184585 | 0.7375726 | -0.1442659 | 0.3923799 | -0.5969306 |
| GB55533 | RNA-binding protein squid-like | 20.856600 | 0.0651253 | 0.0778979 | -0.0906335 | -0.1167986 |
| GB48859 | UPF0160 protein MYG1, mitochondrial-like isoform X2 | 20.818643 | 0.2361138 | 0.2491324 | -0.2080104 | -0.0332518 |
| GB49433 | H/ACA ribonucleoprotein complex subunit 2-like protein | 20.790828 | 0.5517963 | 0.1195184 | -0.1634197 | 0.0024375 |
| GB42237 | N6-adenosine-methyltransferase 70 kDa subunit-like | 20.731214 | -0.0894263 | 0.2756185 | -0.0857468 | -0.0529242 |
| GB46921 | monocarboxylate transporter 12-like | 20.714713 | 0.1807485 | 0.0007541 | -0.1003586 | -0.2148760 |
| GB45596 | elongation of very long chain fatty acids protein 6-like | 20.705352 | 0.5247867 | -0.4973462 | -0.5304114 | -0.5077637 |
| GB50013 | proclotting enzyme | 20.601511 | 0.2512238 | -0.9767295 | -0.5331162 | -0.2907466 |
| GB55263 | putative fatty acyl-CoA reductase CG5065-like | 20.420422 | -0.0329414 | -0.2619832 | -0.8318867 | -0.3621781 |
| GB54404 | elongation of very long chain fatty acids protein AAEL008004-like | 20.311401 | 2.0337166 | -0.0397052 | -0.1819294 | -0.1518170 |
| GB55094 | protein neuralized isoform X3 | 20.264296 | -0.6029457 | 0.1077662 | -0.6403894 | -0.0243416 |
| GB54427 | ribonucleoside-diphosphate reductase subunit M2 isoform X2 | 20.130036 | 0.0040836 | 0.1604850 | -0.0329101 | 0.0177491 |
| GB54538 | uncharacterized protein LOC411248 isoform X5 | 20.086236 | -0.4660266 | -0.2286794 | -0.0025983 | -0.0413626 |
| GB52768 | alkaline phosphatase, tissue-nonspecific isozyme-like isoform X1 | 20.080226 | -0.0170971 | 0.1366385 | -0.0403085 | -0.0385024 |
| GB51580 | long-chain-fatty-acid–CoA ligase ACSBG2 isoform X1 | 20.069108 | -0.0990216 | -0.1748159 | -0.2690449 | -0.1224712 |
| GB50871 | serine/threonine-protein kinase SIK2-like isoform X2 | 19.916686 | 0.0606616 | -0.1441363 | -0.2312372 | 0.2129038 |
| GB53287 | sialin-like isoform X4 | 19.620220 | -0.0297581 | -0.1059771 | -0.1192229 | -0.2783113 |
| GB49653 | probable phosphoserine aminotransferase-like | 19.478348 | 0.4313976 | 0.0935267 | 0.0591799 | -0.0947978 |
| GB47495 | nucleotide exchange factor SIL1-like | 19.344565 | -0.1521038 | 0.1578777 | -0.0097726 | -0.0068981 |
| GB51723 | 60S ribosomal export protein NMD3 | 19.222509 | -0.0712135 | 0.1664404 | 0.1759210 | -0.0663748 |
| GB48628 | RNA-binding protein Nova-1-like isoform X2 | 19.214104 | 0.0515613 | 0.0209321 | -0.5161615 | -0.1714978 |
| GB50626 | phospholipase D3-like isoform X7 | 19.160241 | -0.1767844 | -0.0946056 | -0.1617004 | -0.0368420 |
| GB54331 | cathepsin L-like isoform X2 | 19.064368 | 0.0167944 | -0.0794017 | -0.3784244 | -0.0640108 |
| GB53412 | fatty acid synthase-like | 18.867764 | 1.1288740 | -0.3170657 | 0.5061635 | -0.1800755 |
| GB51753 | uncharacterized protein LOC100576760 isoform X2 | 18.820612 | 0.0773965 | 0.1404132 | -0.0662854 | -0.1625608 |
| 100577899 | DNA replication complex GINS protein SLD5-like | 18.733489 | 0.3469362 | 0.1156921 | -0.2384693 | -0.0444013 |
| GB42899 | uncharacterized protein LOC551133 isoform X2 | 18.387282 | 0.1289445 | 0.0095466 | -0.0099508 | -0.0564785 |
| GB52446 | uncharacterized protein LOC726987 isoform X5 | 18.323554 | -0.5188239 | -0.2066036 | -0.3780834 | -0.1773838 |
| GB52351 | porphobilinogen deaminase-like | 18.239714 | -0.3935509 | -0.0800125 | -0.5113538 | 0.0303557 |
| GB45381 | putative sodium-coupled neutral amino acid transporter 7-like | 18.232994 | 0.2322221 | -0.2991610 | -0.1452851 | -0.1044424 |
| GB41886 | protein transport protein Sec61 subunit alpha isoform 2 | 18.215808 | 0.7287917 | -0.0327566 | -0.2604661 | -0.3382911 |
| GB52153 | U3 small nucleolar RNA-associated protein 15 homolog | 18.207361 | 0.1742820 | 0.1472587 | -0.0709591 | -0.0205023 |
| GB48203 | laminin subunit beta-1 isoform X2 | 18.135401 | -0.0687494 | 0.0552598 | -0.1815586 | -0.5195985 |
| GB51647 | 4-aminobutyrate aminotransferase, mitochondrial-like isoform X2 | 18.132631 | 0.5676800 | 0.0956367 | -0.1094744 | -0.0314973 |
| GB52454 | mitochondrial pyruvate carrier 2-like | 18.031851 | -0.4590473 | 0.0544465 | -0.1848845 | 0.0310854 |
| GB49942 | mitochondrial dicarboxylate carrier-like isoform 1 | 17.737991 | 0.1890512 | -0.0364015 | -0.1444554 | -0.0878453 |
| GB51614 | probable methylthioribulose-1-phosphate dehydratase-like | 17.686800 | -0.0358269 | -0.0730244 | 2.4507128 | 0.0926130 |
| GB41011 | lateral signaling target protein 2 homolog | 17.643002 | -0.0761978 | -0.1736913 | -0.5037217 | -0.0906862 |
| GB49869 | microsomal triglyceride transfer protein large subunit isoform X1 | 17.589998 | 0.1389107 | 0.2371633 | -0.4710017 | -0.8792260 |
| GB55432 | glucosidase 2 subunit beta-like | 17.428805 | 0.4916918 | 0.1151030 | -0.1781667 | 0.0426794 |
| GB40071 | uncharacterized protein LOC410446 | 17.398408 | 0.0764242 | 0.0301336 | 1.2168758 | 0.0847128 |
| GB44888 | MATH and LRR domain-containing protein PFE0570w-like | 17.235171 | 0.0429701 | -0.0248396 | 0.0078619 | -0.1299584 |
| GB54610 | thiamine transporter 2-like, transcript variant X2 | 17.225455 | -0.4767433 | 0.1088769 | -0.1870434 | -0.3209313 |
| GB54661 | phosphoglucomutase isoform X2 | 17.097639 | -0.3363439 | -0.1135590 | -0.1806090 | -0.2087559 |
| GB46422 | proton-coupled amino acid transporter 1 | 16.930428 | 0.2093788 | -0.1884596 | 0.0117507 | -0.1665571 |
| GB45177 | uncharacterized protein LOC725324 isoform X1 | 16.879588 | 0.4068916 | -0.0574424 | -0.1430491 | 0.3385230 |
| GB49633 | RNA 3’-terminal phosphate cyclase-like protein-like isoform X2 | 16.859461 | 0.1575109 | -0.0608420 | -0.0908976 | 0.0954425 |
| GB40141 | venom serine carboxypeptidase | 16.809434 | 0.1223739 | -0.3228364 | -0.3209092 | -0.0884225 |
| GB40280 | pyruvate carboxylase, mitochondrial isoform X1 | 16.742568 | -0.6020803 | -0.0510597 | -0.2153246 | -0.3460215 |
| GB49757 | fatty acid binding protein | 16.704757 | 0.4148758 | -0.1762910 | 0.3588453 | -0.1569230 |
| GB46661 | sodium-independent sulfate anion transporter-like isoform X1 | 16.610634 | -0.2846534 | 0.2134063 | -0.0536858 | -0.0012242 |
| GB45210 | translocon-associated protein subunit gamma-like | 16.589367 | -0.2578927 | -0.0623966 | -0.0363309 | -0.1380282 |
| GB47383 | U4/U6 small nuclear ribonucleoprotein Prp4 | 16.525971 | 0.0183237 | -0.0212914 | -0.0394002 | 0.0668049 |
| GB42787 | dentin sialophosphoprotein-like isoform X4 | 16.515172 | 0.1684747 | 0.3042534 | -0.2740726 | -0.0993491 |
| 102655896 | nucleoplasmin-like protein-like isoform X4 | 16.340267 | 0.1679860 | 0.1843370 | -0.1048845 | 0.0246945 |
| GB55474 | protein pygopus | 16.236962 | 0.2676167 | 0.0707588 | -0.0549138 | 0.0726924 |
| GB51125 | inositol-3-phosphate synthase 1-B isoform X2 | 16.234124 | -0.1324499 | 0.0450646 | -0.1206895 | -0.1431645 |
| GB45968 | collagen alpha-1(IV) chain-like isoform 1 | 16.142244 | -0.1021189 | -0.2851870 | -0.1437885 | -0.1852569 |
| GB44537 | myosin-IA | 16.130906 | -0.3302817 | -0.0513892 | 0.0332848 | -0.1087754 |
| GB45824 | phosphoserine phosphatase isoform X2 | 15.998310 | 0.1362108 | -0.0741826 | -0.1520385 | 0.9771061 |
| GB53567 | branched-chain-amino-acid aminotransferase, cytosolic-like isoform 1 | 15.898775 | -0.1946488 | -0.1506045 | -0.1192245 | 0.0252445 |
| 724293 | protein yellow | 15.838484 | 0.1487303 | -0.2653227 | 0.9050534 | 0.0119983 |
| GB44138 | l-2-hydroxyglutarate dehydrogenase, mitochondrial-like isoform X3 | 15.463787 | -0.0605374 | -0.0645523 | -0.0579366 | -0.0117976 |
| GB45975 | LIM/homeobox protein Lhx3 | 15.448320 | -1.4912892 | 0.1699440 | -0.5350890 | -0.2095720 |
| GB44420 | hydroxymethylglutaryl-CoA synthase 1 isoform X2 | 15.447539 | 0.0319813 | -1.4782209 | -0.2339946 | -0.2200166 |
| GB43942 | putative serine protease K12H4.7-like isoform X2 | 15.444385 | 0.6725080 | 0.0163704 | -0.1396986 | 0.1787550 |
| GB42629 | chromatin accessibility complex protein 1-like | 15.273897 | 0.1251692 | 0.1625803 | -0.0870455 | -0.0091544 |
| GB42541 | carbonic anhydrase-related protein 10-like isoform X3 | 15.217357 | -0.0902229 | -0.2070180 | -0.4223262 | -0.1162996 |
| GB54391 | putative glycogen [starch] synthase-like isoform X1 | 15.171482 | -0.1572320 | -0.1100485 | -0.0326887 | -0.1545854 |
| GB52496 | epoxide hydrolase 4-like isoform X4 | 15.110661 | 0.2774522 | 0.0115722 | -0.3747157 | -0.0800490 |
| GB51598 | translocon-associated protein subunit beta isoform 2 | 14.774053 | 0.5583941 | 0.0371216 | -0.0403127 | -0.1591828 |
| GB49095 | high affinity copper uptake protein 1-like isoformX1 | 14.620522 | 0.5230884 | -0.1010762 | -0.2729704 | -0.0231513 |
| GB54888 | 2-acylglycerol O-acyltransferase 1-like isoform X1 | 14.550168 | 0.6685157 | 0.0466928 | -0.0917668 | -0.1179655 |
| GB42264 | myb-like protein X-like | 14.521676 | -0.6252822 | -0.1368822 | 1.0730476 | -0.0070602 |
| GB45943 | collagen alpha-5(IV) chain | 14.385447 | -0.0141205 | -0.1686619 | -0.0306632 | 0.1661617 |
| GB51236 | acyl-CoA Delta(11) desaturase isoform X2 | 14.282561 | 0.7514364 | 0.0473029 | -0.6010006 | 0.4886544 |
| GB47503 | delta-1-pyrroline-5-carboxylate synthase-like isoform X3 | 14.246721 | -0.4533711 | -0.1181787 | -0.0922763 | -0.0916646 |
| GB47839 | calumenin | 14.227729 | 0.2508064 | 0.1073882 | 1.1338349 | 0.6543477 |
| GB40747 | GMP reductase 2-like isoform 1 | 14.074250 | -0.1389808 | -0.0848805 | 0.0539909 | 0.0060923 |
| GB55661 | neuronal membrane glycoprotein M6-a-like isoform X2 | 13.870018 | 0.2916694 | 0.0445663 | 0.0406151 | 0.0845796 |
| GB49854 | alpha-amylase precursor | 13.835878 | 0.4857671 | 0.0835219 | -1.6759631 | 0.9168179 |
| 726965 | uncharacterized protein LOC726965 | 13.828477 | -0.1511445 | -0.1317802 | 0.1458579 | -0.3221607 |
| 102655415 | uncharacterized protein LOC102655415 | 13.761128 | -0.1886490 | -0.2064529 | -0.8759375 | -0.3895903 |
| GB52114 | protein trachealess-like isoform X7 | 13.706700 | -0.6009081 | -0.0822315 | 2.8207841 | 0.0081549 |
| GB43216 | uncharacterized protein LOC413583 isoform X2 | 13.521796 | -0.2362268 | -0.1658183 | -0.4291904 | -0.6447770 |
| GB47449 | nucleoporin NUP188 homolog | 13.432553 | 0.0398209 | 0.1257927 | -0.3579522 | -0.0552367 |
| GB53230 | adipokinetic hormone receptor | 13.346403 | -0.1559642 | 0.0488804 | -0.4935836 | -0.3911266 |
| GB42738 | protein cueball-like | 13.218575 | 0.0792556 | 0.0187766 | -0.3277604 | -0.1859564 |
| GB42468 | phospholipase B1, membrane-associated-like isoform X1 | 13.019295 | 0.1712758 | -2.6550613 | -0.2391406 | 0.1282518 |
| GB48521 | RNA polymerase II elongation factor ELL2-like isoform X1 | 12.917540 | -0.0107311 | -0.1580317 | -0.1465078 | 0.0207912 |
| GB49321 | D-arabinitol dehydrogenase 1-like | 12.778844 | 0.3850348 | -0.0314272 | -0.1281534 | -0.1467144 |
| GB53404 | protein fork head-like isoform 1 | 12.776526 | -2.0510009 | 0.0551431 | 0.4763584 | -0.2108822 |
| 411557 | protein FAM46A-like isoformX2 | 12.640439 | -0.3724492 | 0.1541695 | -0.1698355 | -0.0530527 |
| GB44850 | origin recognition complex subunit 3-like | 12.544410 | 0.2060399 | -0.0628445 | -0.2511858 | 0.1533299 |
| GB51077 | dystrotelin-like isoform X1 | 12.364985 | -0.2613290 | 0.1545091 | -0.4736396 | 0.0442161 |
| GB49543 | alanine–glyoxylate aminotransferase 2-like | 12.351536 | 0.3435971 | -0.1281697 | -0.1746713 | -0.5539103 |
| GB52712 | serine/arginine repetitive matrix protein 2-like isoform X1 | 12.310149 | 0.1347869 | 0.2130550 | -0.1568323 | 0.1329923 |
| GB53036 | serine/threonine-protein kinase Warts-like isoform X1 | 12.294727 | -0.1758171 | 0.0278491 | -0.2505460 | 0.0098058 |
| GB46917 | uncharacterized protein LOC726071 | 12.249764 | 0.1372400 | 0.0917500 | -0.1651023 | 0.1279429 |
| GB53661 | methyltransferase-like isoform X3 | 12.132568 | -0.2274413 | -0.0795270 | 2.0586400 | -0.0170579 |
| GB51278 | innexin inx3 | 12.091606 | 0.3830713 | 0.0406630 | 0.0169686 | -0.1518675 |
| GB52161 | cuticular protein 28 precursor | 11.933221 | 0.2839393 | -0.6850552 | 0.0492736 | -0.0220819 |
| GB42887 | protein NPC2 homolog | 11.895962 | 0.4934256 | 0.1171569 | 0.8267574 | -0.2535760 |
| GB43984 | xenotropic and polytropic retrovirus receptor 1 homolog | 11.711923 | -0.0394515 | 0.0389923 | 0.0492826 | 0.1485743 |
| GB48252 | dihydrofolate reductase isoform X2 | 11.676320 | 0.2476259 | 0.2239091 | -0.1962494 | 0.1041595 |
| GB47270 | cytochrome P450 4C1 | 11.593087 | 0.3133208 | 0.1872647 | 0.7449695 | 0.5041494 |
| GB48109 | retinoid-inducible serine carboxypeptidase-like isoform X3 | 11.544591 | 0.9904184 | 0.1527256 | -0.4756137 | 0.2243044 |
| GB54313 | uncharacterized protein LOC413386 isoform X3 | 11.417055 | -0.2681125 | 0.0458400 | -0.5743109 | -0.0318130 |
| GB51913 | thymidylate kinase-like isoform X2 | 11.334845 | -0.3730554 | 0.3081842 | -0.1084622 | 0.0965259 |
| GB44503 | uncharacterized protein LOC727423 isoform X2 | 11.287468 | 0.8326731 | -0.2057741 | -0.1159152 | 0.0800218 |
| GB53229 | WAS protein family homolog 1-like | 11.254827 | 0.0009783 | 0.1385308 | 0.0844486 | -0.0924363 |
| GB51834 | sodium-dependent nutrient amino acid transporter 1-like | 11.166136 | -0.3531060 | -0.2620501 | 0.0808984 | 0.0511710 |
| GB52505 | chaoptin-like | 10.968009 | 0.4587636 | -0.0083482 | -0.3768354 | 0.1096745 |
| GB52275 | pancreatic lipase-related protein 2-like | 10.793842 | 0.1098269 | 0.2574445 | -0.4376261 | 0.1596069 |
| GB55302 | trehalose transporter 1 isoform X6 | 10.667963 | -0.0677498 | -0.1155692 | -0.2214355 | 0.3081366 |
| 102654789 | uncharacterized protein LOC102654789 | 10.667109 | -0.0584019 | -0.3278716 | -0.6095776 | 0.0498065 |
| GB42616 | beta-hexosaminidase subunit beta-like | 10.368794 | -0.2289562 | 0.1451877 | 0.0621008 | 0.0620511 |
| GB54153 | uncharacterized protein LOC100576236 isoform X1 | 10.118213 | -0.0809921 | -0.1347052 | -1.4023742 | -0.1316166 |
| GB47327 | lipid phosphate phosphohydrolase 3-like | 10.058571 | 0.2857168 | -0.2176489 | 0.1057685 | -0.0934929 |
| GB50021 | exonuclease 3’-5’ domain-containing protein 2-like isoform X1 | 9.842047 | -0.0736605 | 0.2350361 | 0.2707233 | 0.0938046 |
| GB40344 | uncharacterized protein LOC552242 | 9.828621 | 0.1172944 | -0.8017426 | -0.2242850 | 0.5032930 |
| GB49929 | laminin subunit alpha | 9.561491 | 0.5340516 | 0.2430509 | -0.5370697 | -0.6102948 |
| GB44663 | homeobox protein Nkx-2.4-like | 9.551657 | 0.1394744 | -0.3654465 | 0.1719647 | -0.1904368 |
| GB51107 | uncharacterized protein LOC100578731 isoform X1 | 9.377499 | 0.4302073 | 0.1834154 | 0.1378654 | -0.1713280 |
| GB50524 | uncharacterized protein LOC726417 | 8.929495 | -0.0588231 | 0.0511584 | -1.3909039 | -0.1613334 |
| GB51696 | hexamerin 70c precursor | 8.783477 | -0.0474407 | -0.2625302 | 0.0807997 | 0.5193354 |
| GB51195 | protein abrupt-like isoform X5 | 8.448029 | -0.0648071 | 0.2780828 | -0.3448047 | 0.0069477 |
| GB46800 | uncharacterized protein LOC100577231 | 8.330772 | -0.6305159 | -0.0697162 | 0.5306095 | 0.0739981 |
| GB52656 | uncharacterized protein LOC552154 | 8.299683 | 0.5834384 | -0.2149017 | -0.5531551 | -0.1221217 |
| GB42799 | protein takeout-like | 8.250769 | -0.2869070 | 0.2517661 | -1.5197911 | -1.0284651 |
| GB42426 | glutamyl aminopeptidase-like isoform X2 | 7.939937 | 0.7268796 | 0.4365634 | -0.6505219 | 0.0556743 |
| GB53155 | maternal embryonic leucine zipper kinase-like | 7.859620 | -0.0641905 | 0.0686990 | 3.1684473 | 0.0911321 |
| GB44967 | GTP:AMP phosphotransferase AK3, mitochondrial isoform X1 | 7.715168 | -0.2241576 | -0.0260340 | 1.0680177 | 0.3088382 |
| GB48079 | trypsin-7 | 7.662906 | 0.7889055 | -0.6491093 | -0.9266060 | 0.0966946 |
| 102656088 | uncharacterized protein LOC102656088 | 7.565171 | 1.6565192 | -0.7683197 | -0.7692478 | -0.7298828 |
| GB50434 | proton-coupled amino acid transporter 1-like | 7.268236 | 0.0112121 | -0.1261022 | -0.0116264 | -0.2000854 |
| GB49813 | SUMO-activating enzyme subunit 1 | 7.001295 | 0.5203949 | 0.2339421 | 0.6507883 | 0.1731960 |
| GB43181 | uncharacterized protein LOC552799 isoform X2 | 6.971888 | 0.5939354 | 0.7192746 | -0.8612463 | 0.0416577 |
| GB46693 | WD repeat-containing protein 65-like | 6.867550 | 0.1122710 | -0.0684919 | 0.1286625 | -0.1355103 |
| GB47181 | NADH dehydrogenase [ubiquinone] iron-sulfur protein 4, mitochondrial | 6.863152 | -0.1128277 | -0.0754332 | 0.5035167 | 0.1284447 |
| GB52667 | uncharacterized protein LOC552202 isoform X6 | 6.664971 | -0.2443954 | -0.0018447 | -1.1119964 | -0.0773408 |
| GB53401 | protein fosB isoform X1 | 6.443355 | 0.0228858 | -0.1389772 | 0.0142738 | 0.1133762 |
| GB47507 | histone H2A-like | 6.019835 | -0.6332116 | 0.2794373 | -0.2087029 | -0.1453361 |
| GB45458 | UDP-glucose 6-dehydrogenase-like isoform X2 | 5.705610 | -0.0389463 | -0.0525780 | -0.3343070 | -0.2095720 |
| GB41782 | LOW QUALITY PROTEIN: glycine dehydrogenase [decarboxylating], mitochondrial-like | 5.448141 | 0.1849845 | -0.2525962 | -0.0070789 | -0.1010127 |
| GB54426 | transmembrane protein 205-like | 5.184689 | -0.0505523 | 0.1720915 | 0.0864230 | -0.0824220 |
| GB43591 | uncharacterized protein LOC408443 | 4.927475 | 0.4363105 | 0.2200117 | -0.3238923 | 0.1074204 |
| GB46298 | endocuticle structural glycoprotein SgAbd-8-like isoform X2 | 3.339703 | 0.2037923 | -0.6881852 | -0.0825740 | 0.1612789 |
Table S35: List of all the genes in Module 9, ranked by their within-module connectivity, k. The latter four columns give the Log\(_2\) fold-change in expression in response to queen pheromone in each of the four species.
inspect.module.genes(9) %>%
mutate(am_fc=log2(am_fc), bt_fc=log2(bt_fc), lf_fc=log2(lf_fc), ln_fc=log2(ln_fc)) %>%
rename(Gene=gene, Name=name) %>%
kable.table()
| Gene | Name | k | am_fc | bt_fc | lf_fc | ln_fc |
|---|---|---|---|---|---|---|
| GB49598 | RNA-binding protein Rsf1 | 3.4281703 | 0.3056885 | -0.0032899 | 0.1101417 | 0.0851146 |
| GB49355 | uncharacterized protein LOC100576266 isoform X2 | 3.2620545 | 0.3093869 | 0.0572808 | -0.1561239 | 0.1319324 |
| GB51008 | metaxin-2-like isoform 2 | 3.2002938 | 0.4439731 | -0.1469924 | 0.0424195 | 0.1446767 |
| GB52735 | DAZ-associated protein 2-like isoform X2 | 2.9721946 | 0.2871285 | 0.0231294 | 0.0623909 | -0.1752350 |
| GB55970 | proliferating cell nuclear antigen | 2.8130746 | 0.3776271 | 0.2351576 | 0.0776321 | 0.0776232 |
| 551833 | PAXIP1-associated glutamate-rich protein 1-like isoform 2 | 2.7565876 | 0.4962252 | 0.0926024 | 0.0590149 | 0.2492689 |
| GB43092 | cyclin-dependent kinase 5 | 2.5960809 | 0.3844390 | 0.0216430 | 0.0951021 | 0.1433308 |
| GB55381 | centrosomal protein of 97 kDa isoform X2 | 2.5582953 | 0.2955124 | -0.0548547 | 0.1869490 | 0.1357882 |
| GB43232 | transmembrane protein 222-like isoform 1 | 2.3398175 | 0.5861394 | 0.0458418 | 0.1933063 | 0.2422045 |
| GB50724 | peptidyl-tRNA hydrolase 2, mitochondrial-like isoform 1 | 2.2475846 | 0.7085344 | -0.0764084 | 0.0647428 | 0.1173188 |
| GB51226 | tyrosine-protein kinase CSK isoform X4 | 2.2239789 | 0.5181445 | 0.0036483 | 0.2021335 | 0.1570482 |
| GB56003 | methyltransferase-like protein 14 homolog | 2.2171705 | 0.3353470 | 0.1482768 | 0.1276493 | 0.1038143 |
| GB48128 | DNA-directed RNA polymerase III subunit RPC8-like isoform 1 | 2.1261420 | 0.7927715 | 0.1807240 | -0.1997985 | 0.1943152 |
| GB42319 | uncharacterized protein LOC409105 isoform 1 | 2.1081864 | 0.7613151 | -0.1786302 | 0.0944737 | 0.3063722 |
| GB45649 | adenosine 3’-phospho 5’-phosphosulfate transporter 1 | 2.0383947 | 0.5325883 | -0.0623392 | 0.1488054 | 0.2109308 |
| GB43086 | uncharacterized protein LOC726486 | 1.9692909 | 0.6676944 | 0.0549481 | 0.1238370 | 0.1069750 |
| GB45657 | cdc42 homolog isoform X2 | 1.9443700 | 0.4128119 | 0.1648899 | 0.1727575 | 0.0882596 |
| GB53270 | UPF0428 protein CXorf56 homolog isoformX2 | 1.9439132 | -0.0053964 | 0.0902614 | 0.0955928 | 0.1557436 |
| GB48852 | heterogeneous nuclear ribonucleoprotein H-like isoform X1 | 1.9171405 | 0.3943774 | -0.0242347 | 0.1867469 | 0.1629403 |
| GB45560 | 2-aminoethanethiol dioxygenase-like isoform X2 | 1.8928212 | 0.5646965 | 0.0858905 | 0.2044355 | 0.1964693 |
| GB53957 | U6 snRNA-associated Sm-like protein LSm1-like | 1.8732559 | 1.2758936 | 0.1485275 | 0.0654838 | 0.1025379 |
| GB55241 | myosin-9-like isoform X2 | 1.8577528 | 0.3826838 | 0.0273981 | 0.1613124 | 0.3355618 |
| GB42726 | lysosomal protein NCU-G1-A-like | 1.8538445 | 0.1961158 | -0.1161535 | 0.0827387 | 0.1842311 |
| GB52929 | soluble guanylyl cyclase alpha 1 subunit | 1.8202355 | 0.8632355 | 0.0679563 | 0.2472309 | 0.1991959 |
| GB55098 | progestin and adipoQ receptor family member 4-like isoform X3 | 1.8069386 | 1.0981696 | 0.0958375 | 0.2837369 | 0.3395738 |
| GB50885 | uncharacterized protein LOC409648 | 1.8009421 | 0.5217942 | -0.1408814 | 0.1076250 | -0.0919353 |
| GB54279 | cleavage and polyadenylation specificity factor subunit 4 | 1.7698409 | 0.3124242 | 0.3549593 | 1.6577375 | 0.2521921 |
| GB45810 | locomotion-related protein Hikaru genki isoform X4 | 1.7456427 | 0.4274473 | -0.0495554 | 0.1897961 | 0.1299238 |
| GB54147 | loss of heterozygosity 12 chromosomal region 1 protein homolog | 1.7319102 | 0.4424770 | -0.0518968 | 0.1119449 | 0.0806514 |
| GB48175 | probable cytochrome P450 305a1 | 1.7158930 | 1.5793489 | 0.0957169 | 0.0666737 | 0.2220252 |
| GB50090 | adenosine deaminase acting on RNA | 1.7017820 | 0.2845926 | -0.0201237 | 0.2675177 | 0.3162340 |
| GB55831 | aromatic-L-amino-acid decarboxylase isoform X2 | 1.6395161 | 0.7455077 | 0.7384633 | 0.0929703 | 0.2855078 |
| GB52236 | leucine-rich repeat-containing protein C10orf11 homolog isoform X1 | 1.6041255 | 0.2352825 | 0.0773345 | 0.0243112 | 0.1325469 |
| GB44143 | oxidative stress-induced growth inhibitor 1-like isoform X1 | 1.5781579 | 0.4074280 | 0.0477067 | 0.0904485 | 0.0514744 |
| GB42224 | leucine-rich repeat and calponin homology domain-containing protein 1-like isoform X2 | 1.5751039 | 0.4417497 | -0.0693594 | 1.2318066 | 0.2994614 |
| GB46734 | mitochondrial import inner membrane translocase subunit TIM14-like isoform X3 | 1.5718335 | 0.1173025 | 0.0125511 | 0.2021870 | 0.2728669 |
| GB43817 | atrial natriuretic peptide receptor 1-like | 1.5134486 | 0.4326071 | 0.1235643 | 0.1802794 | 0.0892441 |
| GB50722 | phospholipase A1 member A-like | 0.7527136 | 1.8995474 | 0.3289060 | -0.0744550 | 0.5503768 |
This section shows the operating system and R packages used to produce this document.
sessionInfo() %>% pander()
R version 3.3.2 (2016-10-31)
**Platform:** x86_64-apple-darwin13.4.0 (64-bit)
locale: en_AU.UTF-8||en_AU.UTF-8||en_AU.UTF-8||C||en_AU.UTF-8||en_AU.UTF-8
attached base packages: stats4, parallel, stats, graphics, grDevices, utils, datasets, methods and base
other attached packages: GO.db(v.3.4.0), KEGG.db(v.3.2.3), bindrcpp(v.0.2), knitr(v.1.20), kableExtra(v.0.8.0.0001), pander(v.0.6.0), sva(v.3.22.0), genefilter(v.1.56.0), mgcv(v.1.8-15), nlme(v.3.1-128), MuMIn(v.1.15.6), ecodist(v.1.2.9), gplots(v.3.0.1), ggjoy(v.0.3.0), RColorBrewer(v.1.1-2), gridExtra(v.2.2.1), ggdendro(v.0.1-20), ggrepel(v.0.6.5), ggplot2(v.2.2.1), stringr(v.1.2.0), tidyr(v.0.7.2), dplyr(v.0.7.4), reshape2(v.1.4.3), RSQLite(v.1.1-2), WGCNA(v.1.51), fastcluster(v.1.1.22), dynamicTreeCut(v.1.63-1), GOstats(v.2.40.0), graph(v.1.52.0), Category(v.2.40.0), Matrix(v.1.2-12), AnnotationDbi(v.1.36.2), IRanges(v.2.8.2), S4Vectors(v.0.12.2), Biobase(v.2.34.0) and BiocGenerics(v.0.20.0)
loaded via a namespace (and not attached): bitops(v.1.0-6), matrixStats(v.0.52.2), httr(v.1.3.1), doParallel(v.1.0.10), rprojroot(v.1.2), tools(v.3.3.2), backports(v.1.0.5), R6(v.2.2.2), rpart(v.4.1-10), KernSmooth(v.2.23-15), Hmisc(v.4.0-2), DBI(v.0.5-1), lazyeval(v.0.2.0), colorspace(v.1.3-2), nnet(v.7.3-12), preprocessCore(v.1.36.0), rvest(v.0.3.2), htmlTable(v.1.9), xml2(v.1.2.0), caTools(v.1.17.1), scales(v.0.5.0), checkmate(v.1.8.2), readr(v.1.1.1), RBGL(v.1.50.0), digest(v.0.6.13), foreign(v.0.8-67), rmarkdown(v.1.8), AnnotationForge(v.1.16.1), base64enc(v.0.1-3), pkgconfig(v.2.0.1), htmltools(v.0.3.6), highr(v.0.6), dbplyr(v.1.1.0), htmlwidgets(v.0.8), rlang(v.0.1.4), rstudioapi(v.0.7), impute(v.1.48.0), bindr(v.0.1), gtools(v.3.5.0), acepack(v.1.4.1), RCurl(v.1.95-4.8), magrittr(v.1.5), Formula(v.1.2-1), Rcpp(v.0.12.14), munsell(v.0.4.3), stringi(v.1.1.2), yaml(v.2.1.14), MASS(v.7.3-45), plyr(v.1.8.4), grid(v.3.3.2), gdata(v.2.17.0), lattice(v.0.20-34), splines(v.3.3.2), annotate(v.1.52.1), hms(v.0.3), codetools(v.0.2-15), XML(v.3.98-1.5), glue(v.1.2.0), evaluate(v.0.10), latticeExtra(v.0.6-28), data.table(v.1.10.4-3), foreach(v.1.4.4), gtable(v.0.2.0), purrr(v.0.2.4), assertthat(v.0.2.0), xtable(v.1.8-2), viridisLite(v.0.2.0), survival(v.2.40-1), tibble(v.1.3.4), iterators(v.1.0.9), memoise(v.1.0.0), cluster(v.2.0.5) and GSEABase(v.1.36.0)